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EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards), 2014. Scientific Opinion onthe risk posed by pathogens in food of non-animal origin. Part 2 (Salmonella Yersinia,Shigella and Norovirus in bulb and stem vegetables, and carrots)

EFSA Publication

Link to article, DOI:10.2903/j.efsa.2014.3937

Publication date:2014

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Citation (APA):EFSA Publication (2014). EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards), 2014. Scientific Opinion onthe risk posed by pathogens in food of non-animal origin. Part 2 (Salmonella Yersinia, Shigella and Norovirus inbulb and stem vegetables, and carrots). Europen Food Safety Authority. the EFSA Journal Vol. 12(12) No. 3937https://doi.org/10.2903/j.efsa.2014.3937

https://doi.org/10.2903/j.efsa.2014.3937

https://orbit.dtu.dk/en/publications/cfd8b4eb-a1b8-42b9-8223-89a102d4cdfe

https://doi.org/10.2903/j.efsa.2014.3937

EFSA Journal 2014;12(12):3937

Suggested citation: EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards), 2014. Scientific Opinion on the risk posed

by pathogens in food of non-animal origin. Part 2 (Salmonella Yersinia, Shigella and Norovirus in bulb and stem vegetables,

and carrots). EFSA Journal 2014;12(12):3937, 91 pp. doi:10.2903/j.efsa.2014.3937

Available online: www.efsa.europa.eu/efsajournal

© European Food Safety Authority, 2014

SCIENTIFIC OPINION

Scientific Opinion on the risk posed by pathogens in food of non-animal

origin. Part 2 (Salmonella, Yersinia, Shigella and Norovirus in bulb and

stem vegetables, and carrots)1

EFSA Panel on Biological Hazards (BIOHAZ)2,3

European Food Safety Authority (EFSA), Parma, Italy

ABSTRACT

Bulb and stem vegetables as well as carrots may be minimally processed to obtain ready-to-eat products, and

these steps include selection, washing, cleaning, cutting, packaging and storage. Risk factors for the

contamination of bulb and stem vegetables as well as carrots with Salmonella, Yersinia, Shigella and Norovirus

were considered in the context of the whole food chain. Available estimates of their occurrence in these

vegetables were evaluated together with mitigation options relating to prevention of contamination and the

relevance of microbiological criteria. Emphasis is given to vegetable types associated with public health risks,

i.e. carrots, onion and garlic. It was concluded that each farm environment represents a unique combination of

risk factors that can influence the occurrence and persistence of pathogens in the primary production of these

vegetables. Appropriate implementation of food safety management systems including Good Agricultural

Practices (GAP), Good Hygiene Practices (GHP) and Good Manufacturing Practices (GMP) should be the

primary objectives of producers of bulb and stem vegetables as well as carrots. Considering the limited evidence

for both the occurrence and public health risks from contamination of Salmonella, Shigella, Yersinia and

Norovirus in the primary production and minimal processing of bulb and stem vegetables and carrots, no

conclusions can be made on the impact of the establishment of microbiological Hygiene Criteria, Process

Hygiene Criteria or Food Safety Criteria on public health. There is a lack of data on the occurrence and levels of

Escherichia coli in bulb and stem vegetables as well as carrots. Thus, the effectiveness of E. coli criteria to

verify compliance to GAP, GHP, GMP and food safety management systems (including HACCP) in the

production and minimal processing of bulb and stem vegetables as well as carrots cannot be assessed.

© European Food Safety Authority, 2014

KEY WORDS

bulb and stem vegetables, carrots, microbiological risk factors, Norovirus, Salmonella, Shigella, Yersinia

1 On request from the European Commission, Question No EFSA-Q-2012-00176, adopted on 4 December 2014. 2 Panel members: Olivier Andreoletti, Dorte Lau Baggesen, Declan Bolton, Patrick Butaye, Paul Cook, Robert Davies,

Pablo S. Fernandez Escamez, John Griffin, Tine Hald, Arie Havelaar, Kostas Koutsoumanis, Roland Lindqvist, James

McLauchlin, Truls Nesbakken, Miguel Prieto Maradona, Antonia Ricci, Giuseppe Ru, Moez Sanaa, Marion Simmons,

John Sofos and John Threlfall. Correspondence: [email protected] 3 Acknowledgement: The Panel wishes to thank the members of the Working Group on risk posed by pathogens in food of

non-animal origin Part 2: Ana Allende, Nigel Cook, Paul Cook, James McLauchlin, Christophe Nguyen-The, Birgit

Nørrung and Mieke Uyttendaele for the preparatory work on this scientific opinion and EFSA staff: Maria Teresa da Silva

Felicio and Ernesto Liebana Criado for the support provided to this scientific opinion.

mailto:[email protected]

Salmonella, Yersinia, Shigella and Norovirus in bulb and stem vegetables, and carrots

EFSA Journal 2014;12(12):3937 2

SUMMARY

The European Commission asked EFSA’s Panel on Biological Hazards (BIOHAZ Panel) to prepare a

scientific opinion on the public health risk posed by pathogens that may contaminate food of non-

animal origin (FoNAO). The outcomes of the first and second terms of reference, addressed in a

previous opinion, were discussed between risk assessors and risk managers in order to decide which

food/pathogen combinations should be given priority for the other three terms of reference. This is the

final opinion out of five and addresses the risk from Salmonella, Yersinia, Shigella and Norovirus in

bulb and stem vegetables, and carrots. The terms of reference are to: (i) identify the main risk factors

for bulb and stem vegetables, and carrots, including agricultural production systems, origin and

further processing; (ii) recommend possible specific mitigation options and to assess their

effectiveness and efficiency to reduce the risk for humans posed by Salmonella, Yersinia, Shigella and

Norovirus in bulb and stem vegetables, and carrots, and (iii) recommend, if considered relevant,

microbiological criteria for Salmonella, Yersinia, Shigella and Norovirus in bulb and stem vegetables,

and carrots.

Bulb and stem vegetables, for the scope of this opinion, are defined according to commercial

production and consumption and correspond to the botanically true bulbs of onions (Allium cepa L.,

Allium fistulosum L.), shallot (Allium cepa L.), the composite bulb of garlic (Allium sativum L.); the

bundle of leaf sheath of the leek (Allium ampeloprasum L.); the bulb-like fleshy petioles bases of the

Florence fennel (Foeniculum vulgare Mill.); the young shoots of asparagus (Asparagus officinalis L.);

the fleshy petiole of celery (Apium graveolens L.). Carrots (Daucus carota L.), for the scope of this

opinion, are defined according to commercial production and consumption as a root vegetable,

commonly orange. Emphasis is given here to vegetable types associated with public health risks, i.e.

carrots, onion and garlic.

Bulb and stem vegetables as well as carrots may be minimally processed to obtain ready-to-eat

products, and these steps include selection, washing, cleaning, cutting, packaging and storage. Other

types of minimal processing (e.g. commercial unpasteurized juicing) rarely occur outside retail and

catering. Freezing may take place, but this will typically involve a heat blanching process and is

outside the scope of this opinion, although frozen sliced onion may not be blanched. Bulb and stem

vegetables as well as carrots may be subject to cooking, drying, bottling, canning and other processes

but these are also outside the scope of this opinion.

Despite the variety of types of bulb and stem vegetables as well as carrots produced and consumed,

there is very little or no specific information for interactions with, risk factors, mitigation options and

occurrence of Salmonella, Yersinia, Shigella or Norovirus. Most information is available for

Salmonella and carrots, although this is very limited. Consequently, in addition to the limited data,

conclusions are drawn through what is generally understood about the properties of these pathogens as

well as information from other fresh produce.

Onion, garlic and carrots grow in the soil and stem vegetables such as celery have prolonged direct

contact with soil during growth and/or harvesting, particularly when celery is blanched. When

consumed as ready-to-eat or minimally processed products, these vegetables are normally not

subjected to physical interventions that will eliminate the occurrence of these pathogens.

For the identification of the main risk factors for Salmonella, Yersinia, Shigella and Norovirus

in bulb and stem vegetables and carrots, including agricultural production systems, origin and

further processing, the BIOHAZ Panel concluded that the risk factors at primary production for the

contamination of bulb and stem vegetables as well as carrots with Salmonella, Yersinia, Shigella and

Norovirus are poorly documented in the literature, with limited available data but are likely to include

the following, based on what is known for other pathogens or other fresh produce: (1) environmental

factors, in particular proximity to animal-rearing operation and climatic conditions that increase the

transfer to pathogens from their reservoirs to the bulb and stem vegetables and carrot growing areas;

(2) animal reservoirs (domestic or wild life) gaining access to growing areas for bulb and stem

vegetables or carrots; (3) contamination or cross-contamination by equipment at harvest or post-


EFSA Journal 2014;12(12):3937 3

harvest, and by manipulation by workers if this takes place at primary production; (4) use of untreated

or insufficiently treated organic amendments, and (5) use of contaminated agricultural water either for

irrigation or for application of agricultural chemicals such as pesticides.

Processes at primary production which wet the external portions of the crop close to harvest represent

the highest risk and these include spraying prior to harvest, direct application of fungicides and other

agricultural chemicals and overhead irrigation.

During minimal processing, contamination or cross-contamination via equipment, water or food

handlers are likely to be the main risk factors for contamination of bulb and stem vegetables as well as

carrots with Salmonella, Yersinia, Shigella and Norovirus. There is limited information on the

behaviours of Salmonella, Yersinia, Shigella or Norovirus in the specific vegetable food matrices but

these pathogens are likely to survive on the surfaces of these vegetables for days to several weeks at

both ambient and at refrigeration temperatures.

At distribution, retail and catering and in domestic and commercial environments, contamination and

cross-contamination, in particular via direct or indirect contact between raw contaminated food and

bulb and stem vegetables is a risk factor for Salmonella, Yersinia, Shigella and Norovirus. At

distribution, retail, catering and in domestic or commercial environments, infected food handlers are

also risk factors (particularly for Norovirus and Shigella). Contamination can be direct or indirect via

poor hand hygiene or food contact surfaces. These contamination and cross-contamination risks

include salad bar environments.

For the recommendation of possible specific mitigation options and the assessment of their

effectiveness and efficiency to reduce the risk for humans posed by Salmonella, Yersinia,

Shigella and Norovirus in bulb and stem vegetables, and carrots, the BIOHAZ Panel concluded

that appropriate implementation of food safety management systems including Good Agricultural

Practices (GAP), Good Hygiene Practices (GHP) and Good Manufacturing Practices (GMP) should

be the primary objective of operators producing bulb and stem vegetables as well as carrots. These

food safety management systems should be implemented along the farm to fork continuum and will

be applicable to the control of a range of microbiological hazards.

Salmonella have their reservoirs in domestic as well as wild animals, birds and humans. The main

mitigation options for reducing the risk of contamination of bulb and stem vegetables as well as

carrots are consequently to prevent direct contact with animal, bird or human faeces as well as indirect

contact through slurries, sewage, sewage sludge, contaminated soil, water, equipment or food contact

surfaces or food handlers. Yersinia enterocolitica and Yersinia pseudotuberculosis have their

reservoirs in the intestinal contents of a range of animals and are commonly isolated from different

environments contaminated by faeces. The main mitigation options for reducing the risk of

contamination of bulb and stem vegetables as well as carrots by Yersinia are consequently to prevent

direct contact with animal or human faeces as well as indirect contact through slurries, sewage,

sewage sludge, contaminated soil, water, equipment or food contact surfaces as well as food handlers.

Both Norovirus and Shigella have their reservoir in humans. Therefore, the main mitigation options

are good personal hygiene practices by food handlers during harvest, manual handling during sorting,

packing and at the point of final preparation and food service. In addition, mitigation options include

prevention of contamination from other food types as well as food contact surfaces.

The main sources within the environment from which contamination of food by Norovirus or Shigella

can arise include sewage-contaminated water and sewage sludge. Hence, at primary production

avoiding the use of sewage-contaminated water and inadequately treated sewage sludge, are the main

mitigation options for reducing the risk of Norovirus and Shigella contamination of these vegetables.

Production areas should be evaluated for hazards that may compromise hygiene and food safety,

particularly to identify potential sources of faecal contamination. If the evaluation concludes that

contamination in a specific area is at levels that may compromise the safety of crops, in the event of


EFSA Journal 2014;12(12):3937 4

heavy rainfall and flooding for example, intervention strategies should be applied to restrict growers

from using this land for production of these vegetables until the hazards have been addressed. Each

farm environment (including open field or greenhouse production) should be evaluated independently

as it represents a unique combination of numerous characteristics that can influence occurrence and

persistence of pathogens in or near bulb and stem vegetables as well as carrot growing areas.

Attention should be paid to the selection of the water sources for irrigation, agricultural chemical

application (e.g. fungicide) and in particular to the avoidance of the use or the ingress of water

contaminated by sewage. Both water treatment or efficient drainage systems that take up excess

overflows are possible mitigation options to prevent the additional dissemination of contaminated

water. Risks posed by water should be minimised by assessing the microbial quality of the sources of

water used on the farm for the presence of pathogens. Since Escherichia coli is an indicator micro-

organism for faecal contamination in irrigation water, growers should arrange for periodic testing to

be carried out to inform preventive measures. Appropriate production, treatment, storage,

management and use of manure or sludge is important.

During minimal processing, GMP and food safety management systems (including HACCP) will

assist Salmonella, Yersinia, Shigella and Norovirus risk mitigation strategies. It is recommended that

water used during minimal processing be monitored to assess its microbial quality. When disinfectants

are used in wash water the concentration should be monitored to verify that they are applied

effectively to reduce the potential risk of cross-contamination while avoiding the accumulation of

disinfection by-products.

The main mitigation options for reducing the risk of pathogen contamination of bulb and stem

vegetables and carrots during minimal processing includes scrupulous adherence to hand hygiene by

food handlers at all stages of the supply chain. Employees with symptoms of gastroenteritis should be

excluded from working in food production (i.e. including harvesting and minimal processing) until

their symptoms have subsided. Equipment should be cleaned and disinfected on a regular basis

according to written procedures to ensure that the potential for cross-contamination is minimized. All

persons involved in handling (cutting, grating, dicing, etc.) of bulb and stem vegetables as well as

carrots for buffets in catering and restaurants should receive hygiene training appropriate to their tasks

and receive periodic assessment while performing their duties to ensure tasks are being completed

with due regard to good hygiene and hygienic practices.

Information should be provided to consumers on appropriate handling of bulb and stem vegetables

and carrots, which should include specific directions for product storage, preparation and intended

use. Consumers should be informed if bulb and stem vegetables as well as carrots are intended to be

consumed as ready-to-eat, and to wash and/or scrub whole or peeled products using potable running

water when appropriate.

For the recommendation, if considered relevant, of microbiological criteria for Salmonella,

Yersinia, Shigella and Norovirus in bulb and stem vegetables, and carrots throughout the production chain, the BIOHAZ Panel concluded that there is no routine or regular monitoring of

bulb and stem vegetables or carrots for the presence of Salmonella, Yersinia, Shigella and Norovirus

in the EU Member States and there are limited data on the occurrence of these pathogens in/on these

vegetables in Europe. There are limited studies available in the peer-reviewed world literature on the

occurrence of Salmonella, Yersinia, Shigella and Norovirus on/in bulb and stem vegetables as well as

carrots. There are difficulties in making meaningful comparisons between individual studies as well as

assessing the representativeness of these data to estimate the overall levels of contamination.

Considering the limited evidence for both the occurrence and public health risks from contamination

of Salmonella, Shigella, Yersinia and Norovirus in the primary production and minimal processing of

bulb and stem vegetables and carrots, no conclusions can be made on the impact of the establishment

of microbiological Hygiene Criteria, Process Hygiene Criteria or Food Safety Criteria on public

health.


EFSA Journal 2014;12(12):3937 5

There is a lack of data on the occurrence and levels of E. coli in bulb and stem vegetables as well as

carrots. Thus, the effectiveness of E. coli criteria to verify compliance to GAP, GHP, GMP and food

safety management systems (including HACCP) in the production and minimal processing of bulb

and stem vegetables as well as carrots cannot be assessed.

The BIOHAZ Panel recommended that: (1) more detailed categorization of food of non-animal

origin should be introduced to allow disaggregation of the currently reported data collected via

EFSA’s zoonoses database on occurrence and enumeration of foodborne pathogens; (2) if additional

biological hazards or further public health risks are identified with the consumption of these

categories of food of non-animal origin, risk assessment studies may be needed to inform the level of

hazard control that should be achieved at different stages of the food chain. These studies should be

supported by targeted surveys on the occurrence of foodborne pathogens in such vegetables at specific

steps in the food chain to indicate the level of hazard control and efficacy of application of food safety

management systems, including GAP, GHP, GMP and HACCP, that can be achieved and (3) further

data should be collected to evaluate the suitability of microbiological (e.g. E. coli) indicators for

relevant microbiological hazards in bulb and stem vegetables and carrots during their production and

minimal processing.

Salmonella, Yersinia, Shigella and Norovirus in bulb and stem vegetables and carrots

EFSA Journal 2014;12(12):3937 6

TABLE OF CONTENTS

Abstract .................................................................................................................................................... 1 Summary .................................................................................................................................................. 2 Background as provided by the European Commission ........................................................................... 9 Terms of reference as provided by the European Commission ................................................................ 9 Clarifications of the Terms of Reference 3 to 5 of the request on the risk posed by pathogens in food of

non-animal origin ................................................................................................................................... 10 Background as provided by the European Commission ......................................................................... 10 Terms of reference as provided by the European Commission .............................................................. 11 Assessment ............................................................................................................................................. 12 1. Introduction ................................................................................................................................... 12

1.1. Public health risks associated with bulb and stem vegetables as well as carrots .................. 13 2. Production of bulb and stem vegetables and carrots...................................................................... 16

2.1. Definition of bulb and stem vegetables and carrots .............................................................. 16 2.2. Description of production systems: carrots ........................................................................... 17

2.2.1. Seed and seedling production ........................................................................................... 18 2.2.2. Open field production ....................................................................................................... 18 2.2.3. Water sources and irrigation systems ............................................................................... 18 2.2.4. Different types of fertilisation, organic/manure/compost ................................................. 19 2.2.5. Harvesting ......................................................................................................................... 19 2.2.6. Cooling/post-harvest storage ............................................................................................ 19

2.3. Description of production systems: onions ........................................................................... 20 2.3.1. Seed and seedling production ........................................................................................... 20 2.3.2. Open-field production ....................................................................................................... 20 2.3.3. Greenhouse production ..................................................................................................... 20 2.3.4. Water sources and irrigation systems ............................................................................... 20 2.3.5. Different types of fertilisation, organic/manure/compost ................................................. 21 2.3.6. Harvesting ......................................................................................................................... 21 2.3.7. Cooling/post-harvest storage ............................................................................................ 21

2.4. Description of production systems: garlic ............................................................................ 22 2.4.1. Seed and seedling production ........................................................................................... 22 2.4.2. Open field production ....................................................................................................... 22 2.4.3. Water sources and irrigation systems ............................................................................... 22 2.4.4. Different types of fertilisation, organic/manure/compost ................................................. 22 2.4.5. Harvesting ......................................................................................................................... 23 2.4.6. Cooling/post-harvest storage ............................................................................................ 23

2.5. Description of production systems: celery ............................................................................ 23 2.5.1. Seed and seedling production ........................................................................................... 23 2.5.2. Open field production ....................................................................................................... 23 2.5.3. Greenhouse production ..................................................................................................... 23 2.5.4. Water sources and irrigation systems ............................................................................... 24 2.5.5. Different types of fertilization, organic/manure/compost ................................................. 24 2.5.6. Harvesting ......................................................................................................................... 24 2.5.7. Cooling, post-harvest storage ........................................................................................... 24

2.6. Description of EU bulb and stem vegetables and carrots sector ........................................... 24 3. Risk factors for microbiological contamination during agricultural production ........................... 25

3.1. Environmental factors ........................................................................................................... 25 3.1.1. Factors linked to the adherence, survival and internalisation of pathogens with bulb and

stem vegetables and carrots ........................................................................................................... 26 3.1.2. Conditions in the field and adjacent land ......................................................................... 27 3.1.3. Climatic conditions ........................................................................................................... 27 3.1.4. Contact with animal reservoirs ......................................................................................... 27

3.2. Organic amendments (manure, slurries, composts, wastewater treatment, sludge and

sewage) .............................................................................................................................................. 28


EFSA Journal 2014;12(12):3937 7

3.3. Water use during production (irrigation, pesticides and fertilizers, washing) ...................... 28 3.4. Equipment ............................................................................................................................. 29 3.5. Worker health and hygiene, worker training ........................................................................ 29 3.6. Conclusions ........................................................................................................................... 29

4. Description of minimal processing methods for bulb and stem vegetables and carrots ................ 30 4.1. Onion (washing, peeling and cutting, shredding, packaging) ............................................... 30 4.2. Garlic (washing, peeling, packaging) ................................................................................... 31 4.3. Celery ( washing, peeling, cutting, packaging) ..................................................................... 31 4.4. Carrot (washing, peeling, cutting, packaging) ...................................................................... 31

5. Risk factors for microbiological contamination during minimal processing treatments, including

the main minimal processing practices................................................................................................... 32 5.1. Environmental factors ........................................................................................................... 32 5.2. Water sources (washing and other uses) ............................................................................... 33 5.3. Equipment ............................................................................................................................. 33 5.4. Worker health and hygiene, worker training ........................................................................ 33 5.5. Conclusions ........................................................................................................................... 33

6. Description of the distribution, retail and catering including domestic and commercial

environments for bulb and stem vegetables and carrots ......................................................................... 33 7. Risk factors for microbiological contamination during distribution, retail and catering including

domestic and commercial environments ................................................................................................ 34 7.1. Water sources (washing) ....................................................................................................... 34 7.2. Equipment, worker health and hygiene, worker training ...................................................... 35 7.3. Storage temperature .............................................................................................................. 35 7.4. Conclusions ........................................................................................................................... 36

8. Pathogen occurrence on bulb and stem vegetables and carrots ..................................................... 36 8.1. Salmonella............................................................................................................................. 36

8.1.1. Analytical methods for the detection and enumeration of Salmonella in bulb and stem

vegetables and carrots .................................................................................................................... 36 8.1.2. Data on occurrence and levels of Salmonella on bulb and stem vegetables and carrots .. 36

8.2. Yersinia ................................................................................................................................. 40 8.2.1. Analytical methods for the detection and enumeration of Yersinia in bulb and stem

vegetables and carrots .................................................................................................................... 40 8.2.2. Data on occurrence and levels of Yersinia on bulb and stem vegetables and carrots ....... 40

8.3. Shigella ................................................................................................................................. 42 8.3.1. Analytical methods for the detection and enumeration of Shigella in bulb and stem

vegetables and carrots .................................................................................................................... 42 8.3.2. Data on occurrence and levels of Shigella on bulb and stem vegetables and carrots ....... 42

8.4. Norovirus .............................................................................................................................. 44 8.4.1. Analytical methods for the detection and enumeration of Norovirus in bulb and stem

vegetables and carrots .................................................................................................................... 44 8.4.2. Data on occurrence and levels of Norovirus on bulb and stem vegetables and carrots .... 44

8.5. Conclusions ........................................................................................................................... 45 9. Mitigation options to reduce the risk to humans posed by Salmonella, Yersinia, Shigella or

Norovirus contamination in bulb and stem vegetables and carrots ........................................................ 45 9.1. Introduction ........................................................................................................................... 45 9.2. General mitigation options .................................................................................................... 46

9.2.1. Environment ..................................................................................................................... 46 9.2.2. Manure, sewage and sewage sludge ................................................................................. 47 9.2.3. Water ................................................................................................................................ 47

9.2.3.1. Water in primary production .................................................................................... 47 9.2.3.2. Process wash water .................................................................................................. 48

9.2.4. Equipment ......................................................................................................................... 48 9.2.5. Training and education of workers ................................................................................... 48 9.2.6. Final product ..................................................................................................................... 49 9.2.7. Conclusions ...................................................................................................................... 49


EFSA Journal 2014;12(12):3937 8

9.3. Specific mitigation options to reduce the risk of Salmonella and Yersinia contamination ... 50 9.4. Specific mitigation options to reduce the risk of Shigella and Norovirus contamination ..... 51

10. Data on occurrence of E. coli on bulb and stem vegetables and carrots and use of E. coli as an

indicator .................................................................................................................................................. 53 11. Microbiological criteria for bulb and stem vegetables and carrots ........................................... 53 Conclusions and recommendations ........................................................................................................ 55 References .............................................................................................................................................. 59 Appendices ............................................................................................................................................. 69 Appendix A. List of questions to be addressed by the European Fresh Produce Association

(Freshfel) and information received from Freshfel on 22 July 2013 and 19 August 2014..................... 69 Appendix B. Bulb and stem vegetables and carrots production statistics tables (EUROSTAT,

FAOSTAT) (provided by Freshfel on 19 August 2014 .......................................................................... 80 Glossary .................................................................................................................................................. 88


EFSA Journal 2014;12(12):3937 9

BACKGROUND AS PROVIDED BY THE EUROPEAN COMMISSION

In May 2011 a major outbreak of Shiga toxin-producing Escherichia coli (STEC)4 O104:H4 occurred

in Germany. About 4,000 people were reported ill with symptoms and the outbreak resulted in the

death of more than 56 people. Other countries reported a certain number of people becoming ill by the

same strain, most of whom had recently visited the region of northern Germany where the outbreak

occurred. At the end of June 2011, there was a second cluster in Bordeaux, France, which was caused

by the same Escherichia coli strain. In both cases, investigations pointed to the direction of sprouted

seeds.

According to the 2009 Zoonoses Report,5 the majority of verified outbreaks in the EU were associated

with foodstuffs of animal origin. Fruit and vegetables were implicated in 43 (4.4 %) verified

outbreaks. These outbreaks were primarily caused by frozen raspberries contaminated with Norovirus.

According to the US Centers for Disease Control and Prevention (CDC) 2008 report on surveillance

for food borne disease outbreaks,6 the two main commodities associated with most of the outbreak-

related illnesses originating from food of plant origin were fruits-nuts and vine-stalk vegetables. One

of the main pathogen-commodity pair responsible for most of the outbreaks was Norovirus in leafy

vegetables. The pathogen-commodity pairs responsible for most of the outbreak-related illnesses were

Salmonella spp. in vine-stalk vegetables and Salmonella spp. in fruits-nuts. In addition, as recently as

September 2011, a multistate outbreak of listeriosis linked to cantaloupe melons caused 29 deaths in

the US.

Regulation (EC) No 852/2004 on the hygiene of foodstuffs7 lays down general hygiene requirements

to be respected by food businesses at all stages of the food chain. All food business operators have to

comply with requirements for good hygiene practice in accordance with this Regulation, thus

preventing the contamination of food of animal and of plant origin. Establishments other than primary

producers and associated activities must implement procedures based on the Hazard Analysis and

Critical Control Points (HACCP) principles to monitor effectively the risks.

In addition to the general hygiene rules, several microbiological criteria have been laid down in

Regulation (EC) No 2073/20058 for food of non-animal origin.

Following the STEC O104:H4 outbreak in Germany and France, the Commission already has asked

EFSA for a rapid opinion on seeds and sprouted seeds. EFSA adopted a scientific opinion on the risk

posed by STEC and other pathogenic bacteria in seeds and sprouted seeds on 20 October 2011. The

current mandate intends to supplement the adopted opinion.

In view of the above, there is a need to evaluate the need for specific control measures for certain food

of non-animal origin, supplementing the general hygiene rules.

TERMS OF REFERENCE AS PROVIDED BY THE EUROPEAN COMMISSION

EFSA is asked to issue scientific opinions on the public health risk posed by pathogens that may

contaminate food of non-animal origin such as fruit, vegetables, juices, seeds, nuts, cereals,

mushrooms, algae, herbs and spices and, in particular:

1. To compare the incidence of foodborne human cases linked to food of non-animal origin and

foodborne cases linked to food of animal origin. This ToR should provide an indication of the

4 Also known as Verocytotoxin-producing Escherichia coli (VTEC). 5 EFSA Journal 2011;9(3):2090 6 www.cdc.gov/mmwr/preview/mmwrhtml/mm6035a3.htm?s_cid=mm6035a3_w 7 Regulation (EC) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of

foodstuffs. OJ L 139, 30.4.2004, p. 1-54. 8 Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. OJ L 338,

22.12.2005, p. 1-26.


EFSA Journal 2014;12(12):3937 10

proportionality between these two groups as regard human cases and, if possible, human

burden.

2. To identify and rank specific food/pathogen combinations most often linked to foodborne

human cases originating from food of non-animal origin in the EU.

3. To identify the main risk factors for the specific food/pathogen combinations identified under

ToR 2, including agricultural production systems, origin and further processing.

4. To recommend possible specific mitigation options and to assess their effectiveness and

efficiency to reduce the risk for humans posed by food/pathogen combinations identified

under ToR 2.

5. To recommend, if considered relevant, microbiological criteria for the identified specific

food/pathogen combinations throughout the production chain.

The Commission would like an opinion on the first and second terms of reference by the end of

December 2012. The outcome of the first and second terms of reference should be discussed between

risk assessors and risk managers in order to decide which food/pathogen combinations should be given

priority for the other terms of reference.

CLARIFICATIONS OF THE TERMS OF REFERENCE 3 TO 5 OF THE REQUEST ON THE RISK

POSED BY PATHOGENS IN FOOD OF NON-ANIMAL ORIGIN

BACKGROUND AS PROVIDED BY THE EUROPEAN COMMISSION

On 23 January 2012, a request was provided to the European Food Safety Authority (EFSA) to issue

scientific opinions on the public health risk posed by pathogens that may contaminate food of non-

animal origin (FoNAO).

The BIOHAZ Panel of EFSA adopted during its meeting on 6 December 2012 an opinion on the first

and second terms of reference, focussing on

the comparison of the incidence of foodborne human cases linked to FoNAO and foodborne

cases linked to food of animal origin;

identifying and ranking specific food/pathogen combinations most often linked to foodborne

human cases originating from FoNAO in the EU.

It was agreed in the original request that the outcome of the first and second terms of reference should

be discussed between risk assessors and risk managers in order to decide which food/pathogen

combinations should be given priority for the other terms of reference addressing risk factors,

mitigation options and possible microbiological criteria.

The first opinion of EFSA under this request identifies more than 20 food/pathogen combinations in

its five top ranking groups. The opinion also contains a preliminary assessment of risk factors linked

to certain examples of FoNAO (e.g. tomatoes, watermelons and lettuce), representing specific

production methods for several FoNAO. Several risk factors and mitigation options may be common

for several food/pathogen combinations due to similar production methods. It seems therefore

opportune to combine the risk assessment of such food/pathogen combinations. When risk factors and

mitigation options are identified as more specific to the individual food/pathogen combination, then

these should be considered to supplement this approach and added where possible within the,

opinions. Alternatively, it is worth mentioning that a reference could be made if such specific risks

have already been addressed in previous opinions.


EFSA Journal 2014;12(12):3937 11

TERMS OF REFERENCE AS PROVIDED BY THE EUROPEAN COMMISSION

EFSA is asked, in accordance with article 29 of Regulation (EC) No 178/2002,9 to provide scientific

opinions on the public health risk posed by pathogens on food of non-animal origin as regards risk

factors, mitigation options and possible microbiological criteria. When considered more appropriate

e.g. because of low prevalence of the pathogen or in view of a broader process control, indicators may

be proposed as Process Hygiene Criteria. When addressing mitigation options at primary production,

attention should be paid to Article 5(3) of Regulation (EC) No 852/2004,10

which laid down that the

application of hazard analysis and critical control points (HACCP) principles shall only be applied to

food business operators after primary production and associated activities.11

This provision does,

however, not exclude proposing microbiological criteria in accordance with terms of reference 5 when

considered relevant.

EFSA is requested to provide opinions in line with the agreed terms of Reference 3 to 5 (EFSA-Q-

2012-00237) for the following food/pathogen combinations with a similar production system:

(1) The risk from Salmonella and Norovirus in leafy greens eaten raw as salads.

Cutting and mixing before placing on the market should be included as potential risk factor and

specific mitigation options proposed if relevant.

(2) The risk from Salmonella, Yersinia, Shigella and Norovirus in bulb and stem vegetables, and

carrots.

(3) The risk from Salmonella and Norovirus in tomatoes.

(4) The risk from Salmonella in melons.

(5) The risk from Salmonella and Norovirus in berries.

9 OJ L 31, 1.2.2002, p.1 10 Regulation (EC) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of

foodstuffs. 11 See guidance at: http://ec.europa.eu/food/food/biosafety/hygienelegislation/guidance_doc_852-2004_en.pdf

http://ec.europa.eu/food/food/biosafety/hygienelegislation/guidance_doc_852-2004_en.pdf


EFSA Journal 2014;12(12):3937 12

ASSESSMENT

1. Introduction

Bulb and stem vegetables as well as carrots can be consumed as minimally processed, ready-to-eat

food, which are widely eaten and usually free from noxious substances such as poisonous chemicals,

toxins and pathogenic micro-organisms. However, a previous EFSA opinion (EFSA Panel on

Biological Hazards (BIOHAZ), 2013a), carried out a risk ranking exercise for identifying the relative

importance of combinations of food of non-animal origin (FoNAO) and pathogens linked to outbreaks

of foodborne illness in the EU. Leafy greens eaten raw as salads and Salmonella were ranked as the

most important (EFSA Panel on Biological Hazards (BIOHAZ), 2013a), but this analysis ranked the

combination of: bulb and stem vegetables together with Salmonella as amongst the second most

important combinations, together with bulb and stem vegetables and Norovirus as one of the fourth

most important combinations. Furthermore, the same analysis (EFSA Panel on Biological Hazards

(BIOHAZ), 2013a) risk ranked the combinations of carrots both with Yersinia as amongst the fourth

most important, and with Shigella as one of the fifth most important groups.

The main risk factors for microbiological risks, together with their mitigation options, are applicable to

many points in the food chain for bulb and stem vegetables and carrots. However since the supply

chains of bulb and stem vegetables and carrots may not include processing steps or control points

which will ensure inactivation or removal of biological hazards, it is particularly important to consider

risk factors (and consequentially mitigation options) at the point of production, (minimal) processing,

storage and retail or catering. This is similar to other foods of non-animal origin, which are minimally

processed and often sold as ready-to-eat, as well as with some foods of animal origin (e.g.

unpasteurised dairy products, shellfish and meats), which are also eaten raw or minimally processed.

The approaches used in this opinion are:

1. To provide a descriptive analysis of the whole production process for a representative range

of bulb and stem vegetables and carrots which considers their origins in agricultural

production, growing, harvesting, minimal processing, distribution, retail, catering and

handling in domestic environments. Emphasis will be given to descriptions of vegetable

types associated with public health risks. Risk factors for contamination by Salmonella,

Yersinia, Shigella and Norovirus are considered in the context of the agricultural production,

minimal processing, distribution and retail/catering/domestic environments. In discussions

with the European Commission it was agreed that for all the FoNAO considered in this and

the related opinions, only minimally processed products are considered (which includes

cutting, washing, peeling, shredding, freezing, mashing and unpasteurized juicing). Products

undergoing thermal treatments (including heat blanching as well as shelf-stable juicing) and

other processing treatments (such as pickling, canning, bottling, drying or powdering), as

well as composite foods containing these vegetables are not considered in the scope of these

opinions.

2. This opinion includes separate Sections, which assess specific mitigation options to reduce

contamination of bulb and stem vegetables and carrots by Salmonella, Yersinia, Shigella and

Norovirus which reduces the risk of exposure through food consumption. Assessment of the

mitigations options is performed in a qualitative manner similar to that performed for the

scientific opinion on the risk posed by Shiga toxin-producing Escherichia coli (STEC) and

other pathogenic bacteria in seeds and sprouted seeds (EFSA Panel on Biological Hazards

(BIOHAZ), 2011c), and include consideration of generic mitigation options previously

identified for leafy greens eaten raw as salads (EFSA BIOHAZ Panel, 2014a), berries (EFSA

BIOHAZ Panel, 2014b), melons (EFSA BIOHAZ Panel, 2014e) and tomatoes (EFSA

BIOHAZ Panel, 2014d). Emphasis is given here to vegetable types associated with public

health risks, i.e. carrots, onion and garlic.


EFSA Journal 2014;12(12):3937 13

3. Sampling and analytical methods for the detection of Salmonella, Yersinia, Shigella and

Norovirus (together with the use of E. coli as an indicator organism) in bulb and stem

vegetables and carrots are considered similarly to those identified for leafy greens (EFSA

BIOHAZ Panel, 2014a) berries (EFSA BIOHAZ Panel, 2014b), melons (EFSA BIOHAZ

Panel, 2014e) and tomatoes (EFSA BIOHAZ Panel, 2014d). Summaries of available data on

estimates of occurrence for Salmonella, Yersinia, Shigella, E. coli and Norovirus in bulb and

stem vegetables and carrots are presented. The relevance of microbiological criteria

applicable to production, minimal processing and at retail/catering was considered.

Microbiological criteria in domestic settings were not considered.

1.1. Public health risks associated with bulb and stem vegetables as well as carrots

Previous risk ranking analysis used data from foodborne outbreaks reported as part of the zoonoses

monitoring (Directive 2003/99/EC)12

in the EU between 2007 and 2011 (EFSA Panel on Biological

Hazards (BIOHAZ), 2013a). Outbreaks having a strong or moderate strength of association with

consumption of raw or minimally processed bulb or stem vegetables or carrots were as follows:

Carrots and

o Yersinia pseudotuberculosis, 2008, Finland, 50 cases

o Shigella, 2008, Sweden, 145 cases

o Norovirus, 2009, Belgium, 2 cases

Onion and

o Salmonella enterica serovar Haifa, 2011, Sweden, 30 cases

o Norovirus, 2011, Finland, 16 cases

Garlic (water used for brushing langos) and

o Norovirus, 2010, Germany, 2 cases

Some of the above outbreaks are further documented in the peer-reviewed literature: carrots

contaminated with Y. pseudotuberculosis (Kangas et al., 2008; Vasala et al., 2014) and carrots

contaminated with Norovirus (Kaminska et al., 2014). Additional information is available for

outbreaks in the EU which occurred outside the previous 2007-2011 study period (EFSA Panel on

Biological Hazards (BIOHAZ), 2013a) and were associated with: Y. pseudotuberculosis infection and

consumption of grated carrots which occurred in 2003 and 2006 (111 and > 400 cases respectively

(Jalava et al., 2006; Rimhanen-Finne et al., 2009); and Norovirus and frozen carrots in 2012, Poland,

97 cases (Kaminska et al., 2014); four Norovirus outbreaks associated with consumption of carrots

(one outbreak of 122 cases in Sweden in 2012; and the remaining three outbreaks in Germany in 2012

and 2013 with 2, 2, and 5 cases respectively).

In addition, an outbreak has been reported within the EU with these types of food products and other

biological hazards, namely: grated carrots with red peppers and Cryptosporidium hominis in Denmark

(Ethelberg et al., 2009). Outbreaks have been reported with these types of food products outside the

EU and included: enterotoxigenic E. coli and chives in Norway (Macdonald et al., 2014); spring onion

(also known as scallions or green onions) and hepatitis A virus in the USA (Dentinger et al., 2001;

Wheeler et al., 2005); diced celery and Listeria monocytogenes in the USA (Gaul et al., 2013); raw

12 Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 on the monitoring of zoonoses

and zoonotic agents, amending Council Decision 90/424/EEC and repealing Council Directive 92/117/EEC. OJ L 325,

12.12.2003, p. 31-40.


EFSA Journal 2014;12(12):3937 14

carrots and Shigella sonnei in the USA (Gaynor et al., 2009); carrots and Salmonella enterica serovars

Branderup and Typhimurium in the USA (Hanning et al., 2009); raw celery and Norovirus in the USA

(Warner et al., 1991); raw celery/tomatoes/lettuce and Listeria monocytogenes in the USA (Ho et al.,

1986); and fresh garlic and Salmonella enterica serovar Virchow in Australia (Bennett et al., 2003).

In consultation with the European Commission and, based on documented public health risks, the

approach used in this opinion will focus on descriptions of production systems, risk factors and

mitigation options for the foods and pathogens outlined in Table 1 from EFSA Panel on Biological

Hazards (BIOHAZ) (2013a). Other bulb and stem vegetable types will be briefly considered if these

have been associated with public health risks. This approach allows more general recommendations

covering similar production cycles, risk factors and mitigation options for this group of vegetables

consumed raw or minimally processed.


EFSA Journal 2014;12(12):3937 15

Table 1: Food pathogen combinations identified in EFSA Panel on Biological Hazards (BIOHAZ) (2013a) based on strong or moderate associations with

foodborne outbreak data reported in the EU from 2007 to 2011 associated with raw or minimally processed bulb and stem vegetables and carrots

Pathogen Food vehicle(a)

Setting(b)

Place of origin of problem(c)

Contributory factors(d)

Salmonella enterica serovar

Haifa Onion

Disseminated cases Unknown Unprocessed contaminated ingredient

Yersinia pseudotuberculosis Raw grated carrot School kindergarten Farm (primary production) Unprocessed contaminated ingredient

Shigella Raw grated carrots Restaurant, cafe, pub, bar, hotel Catering services, restaurant Infected food handler

Norovirus Garlic water used for

brushing lángos

Restaurant, cafe, pub, bar, hotel Restaurant, cafe, pub, bar,

hotel, catering services

Cross-contamination, infected food handler,

unprocessed contaminated ingredient

Norovirus Chopped onion Household, domestic kitchen Restaurant, cafe, pub, bar,

hotel, catering services

Infected food handler

Norovirus Carrots Residential institution (nursing

home, prison, boarding school)

Catering services, restaurant Not reported

(a): Available information reported on the food vehicle.

(b): Place of exposure to the food vehicle. This is the location where the food was consumed or where the final stages of preparation of the food vehicle took place (e.g. café/restaurant,

institution, home, take-away outlet).

(c): Place, other than setting, where the mishandling of the food took place and/or where the contamination occurred.

(d): Contributing factors are factors that contributed to the occurrence of the foodborne outbreak. These may include deficiencies in food handling or contaminated raw materials.


EFSA Journal 2014;12(12):3937 16

2. Production of bulb and stem vegetables and carrots

2.1. Definition of bulb and stem vegetables and carrots

True bulbs are normally formed underground on the basis of modified leaves, consisting of a

succession of layers of scales surrounding the sprout. The scales occur on a very short, compacted

stem, the “stem plate” on which are attached the roots. These vegetables include a high diversity of

products and the size, shape and colour can vary depending on the species of plant and cultivar. Bulbs

are usually produced by biannual plants which enter into dormancy during the winter. Some plants,

such as onion or garlic, can also produce aerial small bulbs. Only bulbs and vegetables consumed raw

or minimally processed are considered here.

Bulb and stem vegetables for the scope of this opinion, are defined according to commercial

production and consumption and correspond to the botanically true bulbs of onions (Allium cepa L.,

Allium fistulosum L.), shallots (Allium cepa L.), the composite bulb of garlic (Allium sativum L.); the

bundle of leaf sheath of leek (Allium ampeloprasum L.); the bulb-like fleshy petiole bases of the

Florence fennel (Foeniculum vulgare Mill.); the young shoots of asparagus (Asparagus officinalis L.);

and the fleshy petiole of celery (Apium graveolens L.).

Carrots (Daucus carota L.), for the scope of this scientific opinion, are defined according to

commercial production and consumption as a root vegetable which is commonly orange, although

others colours such as purple, red, white and yellow occur. The edible part of the carrots is developed

underground and includes the root. Carrots are storage organs, principally of carbohydrates. They

generally have low respiration rates although it will depend on the stage of development. Thus, they

are considered relatively non-perishable, especially if the tops are removed. Carrots will continue

growing after harvest (rooting and sprouting); and can be stored for relatively long periods. Only

carrots consumed raw or minimally processed are considered here.

Bulb and stem vegetables were previously defined to include: asparagus, cardoon, celeriac, celery,

elephant garlic, Florence fennel, garlic, kohlrabi, kurrat, leek, lotus root, nopal, onion, Prussian

asparagus, shallot, spring onion and welsh onion (EFSA Panel on Biological Hazards (BIOHAZ),

2013a).

Carrots were previously defined to include: baby carrots, carrot coins, (unpasteurised) juice, sticks,

grated, shredded and sliced carrots (EFSA Panel on Biological Hazards (BIOHAZ), 2013a).

Onions cover a wide diversity of different produce, and for this opinion, are classified according to the

production season and day length required to initiate bulb formation, as long-day, short-day, or

intermediate-day types (UK cooperative extension service, 2013). For market considerations, onions

are also classified according to their colour (white or red bulbs), taste (having pungent or sweet

flavours) and shape (with globes, elongated globes, spindle, flat, yellow) (UK cooperative extension

service, 2013; UGA extension, 2014). For the purpose of this opinion, two main categories will be

considered.

Onions produced as mature bulbs, covered with dry papery leaves (also called scales or skins),

which can usually be stored for several months. A wide range of cultivars is used, including

yellow, red, white, sweet onions (UK cooperative extension service, 2013). All these cultivars

belong to the species Allium cepa L.

Onions produced as immature bulbs attached to fresh tubular leaves. Bulbs can be of various

sizes, and are fully formed to very slender (Chambre d’Agriculture Lot-et-Garonne, 2010).

They are sold under different names such as green onions, spring onions, salad onions, welsh

onion, scallions, and are usually presented at retail sale as bunches. The cultivars used to

produce these immature bulbs can belong to Allium cepa L., the same species as used to


EFSA Journal 2014;12(12):3937 17

produce mature onions, and in such cases are harvested at an early stage. Alternatively, other

onion species can be grown for this use, i.e. Allium fistulosum L. (Oregon State University,

2002a; Ariyama and Yasui, 2006). Chives (Allium schoenoprasum L.) are the smallest onion

type consumed and only the leaves are used, however these are out of scope for this opinion as

these were previously categorised as a fresh herb (EFSA Panel on Biological Hazards

(BIOHAZ), 2013a).

All types of onions can be eaten without cooking, although this is most common for green onions and

sweet cultivars of mature onions. With respect to this opinion, the most important distinction lies

between mature onions and green (immature) onions. Leeks are also occasionally consumed raw or

minimally processed.

Garlic bulbs are formed of 5-20 “cloves” each representing a bud (or a small bulb) formed of 2 scales,

one outside scale which is dry and papery, one internal fleshy scales containing water and nutrients for

the sprout. Garlic represents a less diverse product than onions (Larousse Agricole, 2002). The main

differences are autumn cultivars (planted in autumn) and spring cultivars (planted in end of winter-

early spring). Spring cultivars produce smaller bulbs, which can be stored longer than autumn cultivars

(Chambre d’Agriculture de la Haute-Garonne, 2004). Bulbs can be white (both types of cultivars),

purple (autumn cultivars) or pink (spring cultivars) (Chambre d’Agriculture de la Haute-Garonne,

2004).

Commercially produced carrots usually consist of roots of deep orange colour. Nantes-type cultivars

are commonly grown in Europe and have sparse foliage that is attached to the crown of this vegetable.

The root is moderately long (usually 15 and 20 cm), with a uniform diameter along the length and a

rounded tip when mature (CALU, 2007). The surface is thin and easily damaged. The highly

pigmented core is poorly developed making roots brittle. Nantes cultivar is the most common type

used for the fresh-cut minimal processing (Appendix A, Freshfel information). The Nantes cultivar is

less suitable for long-term storage than other cultivars such as Chantenay and Danvers owing to the

fact that roots have higher sugar content, lower in terpenoids and lower dry matter (Appendix A,

Freshfel information).

Bulb and stem vegetables as well as carrots can be consumed after processing (cooking, pickling,

pasteurised juicing, drying etc.), but these are out of the scope of this opinion. These vegetables are

also consumed as whole or as fresh-cut products (including those sliced, diced and grated). Fresh

juices may also be prepared for immediate consumption (see Section 6). Despite the variety of types of

bulb and stem vegetables as well as carrots produced and consumed, there is very little or no specific

information for interactions with risk factors, mitigation options and occurrence of, Salmonella,

Yersinia, Shigella or Norovirus. Most information is available for Salmonella and carrots, although

this is very limited. Consequently, in addition to the limited data, conclusions are drawn from what is

generally understood about the properties of these pathogens as well as information from other fresh

produce.

Celery has been associated with foodborne outbreaks in the USA (Ho et al., 1986; Warner et al., 1991)

and will be used to describe additional production systems for bulb and stem vegetables other than

those listed in Table 1. The aerial organ of celery is consumed (although this is often blanched by

covering with soil), and is different from mature onion, garlic and carrots where the edible portions

grow within or on the surface of the soil. Among bulb and stem vegetables, celery will illustrate the

case of “stem vegetables”, although what is currently called the celery “stem” or “stalk” is botanically

made up of leaves and petioles.

2.2. Description of production systems: carrots

Carrots are a cool-season crop, but will tolerate warm temperatures early in the growing season. Roots

attain optimal colour when the air temperature is 18 to 21 ºC (Nunez et al., 2008). Root colour can

deepen rapidly when temperatures are within this range 3 weeks before harvest. Above 30 ºC, the


EFSA Journal 2014;12(12):3937 18

growth of foliage is reduced and strong flavours develop in the roots, reducing their market quality.

Below 10 ºC, carrot roots and foliage grow slowly. Carrots tolerate some frost (Nunez et al., 2008).

2.2.1. Seed and seedling production

Carrots are always directly seeded in soil. Both raw and pelleted seeds are used (Nunez et al., 2008).

The ideal sowing time is March/April, about 2 weeks before the last frost is expected. However, it is

possible to establish a “forced crop” which is sown as early as February using cold frames or cloches

for protection. If sown in October, a fleece or plastic cover is needed over winter (CALU, 2007). In

Europe, seeding is done mechanically. Usually, the seeds are sown in beds with sufficient water to

allow growth (Appendix A, Freshfel information). Between rows spacing is 15 to 30 cm with approx.

100 carrots per m2. Higher densities are used for plantings for the fresh-cut market. When beds are

used then more seeds should be placed on the outside rows of the beds. Seeds are sown about 2 cm

deep with a precision drill. The ideal soil temperature for germination is 10 °C (CALU, 2007). Seed

within a lot might vary significantly in size, maturity, vigour and germination time; emergence often

occurs over several days (Nunez et al., 2008).

2.2.2. Open field production

The optimum soil types to grow carrots are clay-loamy soils, which provide the best combination of

water-holding capacity and drainage, although carrots are also grown on sandy soils. Heavy soils can

encourage hairy, deformed roots. Carrots can be successfully produced in both acid and alkaline soils.

However, a pH above 6.0 has been recommended for successful establishment. The structure of the

soil is also important (Appendix A, Freshfel information). It is recommended that the upper 75 cm of

soil should be uniform and free of barriers to root growth (Nunez et al., 2008). To avoid getting forked

roots, the soil should be stone-free for cultivation (CALU, 2007). Thus, the analysis of the soil is

needed to determine its suitability (Appendix A, Freshfel information). Light, well-drained and peaty

soils are ideal. High organic matter content is recommended but it should be ensured that farmyard

manure is well composted and is applied a few months before planting to avoid getting forked roots.

As the carrot root matures, carotene accumulates, causing the root to change from yellow-white to

yellow and then orange. Although cultivars differ in their potential for orange colour, soil fertility,

temperature, and water content are the main factors influencing root colour. The health of the leaves

plays a minor role in root colour unless the tops are severely stressed (Nunez et al., 2008).

It is important to maintain the levels of soil moisture because, if moisture levels decline and the root

tops are exposed to the sun, carrots are vulnerable to “green shoulder” and develop a bitter taste.

Covering with fleece or plastic covers or, traditionally, with straw might also be necessary as shelter

when temperatures are low (CALU, 2007).

2.2.3. Water sources and irrigation systems

A uniform water supply is critical for good colour and root formation. If significant wet-dry cycles

occur, the roots will split. Excessive watering discourages good colour formation and may encourage

plant disease (Nunez et al., 2008). It has been established that carrots require 20-25 mm of rainfall per

week during the growing season but under warm, dry conditions up to 50 mm will be required.

Overhead systems or sprinkler lines are mainly used for irrigation if required (CALU, 2007).

Therefore, fields have to be equipped with irrigation systems and the crop is irrigated lightly,

immediately after sowing. Sometimes, irrigation is needed over the season from the sowing to the

harvest (Appendix A, Freshfel information). Under warm, dry conditions, irrigation water should be

applied once or twice a day. Watering should be gradually reduced to prevent longitudinal splitting of

the roots when the crop approaches maturity. Water stress during root development also causes

cracking of the roots, which also become hard.


EFSA Journal 2014;12(12):3937 19

2.2.4. Different types of fertilisation, organic/manure/compost

Growers use fertilizers and pesticides to increase the production yield (Appendix A, Freshfel

information). Carrot is a comparatively deep-rooted crop compared to other vegetables, and is able to

efficiently extract nitrogen from soil to a depth of several feet. Seasonal nitrogen application varies

widely among growers and fields, ranging from as low as 110 kg/ha to 280 kg/ha. Research has shown

that seasonal nitrogen rates greater than 170 kg/ha are seldom necessary to maximize root yield, and

that excessive nitrogen application increases root cracking during harvest and handling (Nunez et al.,

2008).

Fertiliser recommendations should be based on soil analyses. A small amount of nitrogen is typically

applied before sowing with phosphorus fertilizer, with the majority of nitrogen applied either as a side

dressing or through sprinkler irrigation (Nunez et al., 2008). Organic fertilizers can represent a source

of foodborne pathogens if not adequately treated (EFSA BIOHAZ Panel, 2014c). Manure from

various sources can be used but they should be applied a few months before sowing or planting,

ideally with a different crop between manure application and carrot production.

2.2.5. Harvesting

To determine the optimum time for harvesting, growers take samples from different points of the plot,

including from the leaves, to determine the maturity stage of the root: the leaf quality is an important

parameter (Appendix A, Freshfel information). However, in most cases, harvest decisions for carrots

are based on criteria depending on the market outlet or sales endpoint. Typically carrots are harvested

at an immature state when the roots have achieved sufficient size to fill in the tip and develop a

uniform taper. Length may be used as a maturity index for harvest timing of ‘cut and peel' carrots to

achieve a desired minimal processing efficiency (Suslow et al., 2002).

In Europe, almost all carrots are mechanically harvested. Commercially grown carrots are harvested

using self-propelled multi-row harvesters (Nunez et al., 2008). Careful handling is necessary to avoid

bruising or breaking the roots, thus avoiding mechanical damage. Harvest season is usually between

September and October, but if harvest is carried out when the environment is too wet, it can be

detrimental for quality (Appendix A, Freshfel information). To avoid exposing the roots to heat,

harvesting it is often done after sunset. Also, it is not recommended to leave harvested carrots for too

long on the field, as they will attract carrot fly (CALU, 2007).

2.2.6. Cooling/post-harvest storage

Carrots are harvest in September-November and they can be stored until the following June. As carrots

can develop a ‘rubbery’ texture relatively easy it is necessary to store them below 5 °C. Cold storage is

typically carried out at 2 ºC and 95 % relative humidity (RH) (Appendix A, Freshfel information).

High relative humidity is essential to prevent desiccation and loss of crispness. However, common

storage conditions rarely achieve the optimum temperature for long-term storage to prevent decay,

sprouting, and wilting. At storage temperatures of 3-5 °C, mature carrots can be stored with minimal

decay for 3-5 months (Suslow et al., 2002). In some parts of Europe carrots can be stored up to

9 months (Appendix A, Freshfel information).

To store carrots, green leaves are removed, however the soil remains on this vegetable. After storage,

the soil is removed by dry brushing; carrots are washed and finally packed and sold to the consumers.

When produced on a large scale, washing of the carrots after harvest is done in a washing line. The

first step uses a washing bath where carrots are washed for up to 4 hours. The washing tank consists of

a tank where the water is refreshed occasionally. After the washing tank, carrots are rinsed with

shower water and go via a conveyor belt to packing. Carrots are not dried and are maintained as much

as possible in water (Appendix A, Freshfel information). Careful handling of carrots during and after

harvest prevents bruising, shatter-cracks, and tip breaks and prolongs storage life. Free moisture from

the washing process or condensation, commonly obtained if stored within plastic bags, will promote

vegetable decay (Suslow et al., 2002).


EFSA Journal 2014;12(12):3937 20

After washing, packed carrots can be successfully stored for a further 2-3 weeks at 3-5 °C. However,

carrots can also be sold in bunches tied together including the shoots (CALU, 2007). Bunched carrots

are highly perishable due to the presence of the shoots, but can be maintained for 8-12 days (Suslow et

al., 2002).

Exposure to ethylene will induce the development of a bitter flavour due to isocoumarin formation.

Exposure to as little as 0.5 ppm exogenous ethylene will result in a perceptible bitter flavour, within

2 weeks under normal storage conditions. Thus, carrots should not be mixed with ethylene-producing

commodities such as apples, bananas, tomatoes etc. (Suslow et al., 2002).

2.3. Description of production systems: onions


Sowing can be done with seeds or bulbils (small bulbs). Bulbils permit a more rapid growth of the

plant but are restricted to fewer cultivars than seeds (LPC bio, 2013). Sowing is usually done from

March to May with harvest from August to October, a later sowing and harvest being preferable for

onions intended for a long storage (LPC bio, 2013). In “winter culture”, sowing is done at the end of

summer or in October and harvest in late spring or summer (Verolet, 2001; Chambre d’Agriculture

Rhônes-Alpes, 2012). Seeds can also be sown to produce small plants, which are transplanted as soil

balls (produced with 3-5 seeds per ball), frequently in soil covered by mulch or plastic lining to limit

weeds development (Chambre d’Agriculture Rhônes-Alpes, 2012). Green onions are produced

similarly with a shorter production cycle, with sowing or transplanting from March to July and

harvesting from July to October. For “winter culture” green onions can be sown in September and

harvested in April (Chambre d’Agriculture Rhônes-Alpes, 2012).

2.3.2. Open-field production

All types of onions can be grown in open fields. For mature onions, the soil must be prepared to obtain

a uniform structure for the first 2-5 cm. Deep soil that retains water is preferred. Onion crops never

fully cover the soil and are therefore very sensitive to weeds (UGA extension, 2014). Apart from

chemical herbicides, several techniques are used to reduce or prevent the growth of weeds, including

covering the growing areas before soil preparation for the onion crop, successions of delays and

mechanical destruction of weeds before sowing or planting onions, application of heat before and after

sowing or planting (Chambre d’Agriculture Rhônes-Alpes, 2012; LPC bio, 2013). The impact of these

practices on the survival of foodborne pathogens present in the soil is not known.

2.3.3. Greenhouse production

Greenhouse production is particularly important to obtain green onions in winter (Civam Bio des

Pyrénées-Orientales). Greenhouse production is less important for mature onions which are stored for

several months and harvested from spring to autumn (using cultivars of different precocity and for

which bulb formation is initiated for different day lengths). Greenhouse onion crops usually come

from transplants. In an EU Mediterranean climate in unheated greenhouses for instance, the small

plants (obtained from seeds in approximately one month) can be transplanted as soil balls covered by

plastic lining from September to January and green onions harvested from the beginning of January to

April. Greenhouses must be very well ventilated to avoid excess humidity, which will increase the risk

of onion disease development (Civam Bio des Pyrénées-Orientales). The requirements concerning

weeds control, fertilization and irrigation are the same as for open-field cultivation.


Onions need very well controlled water supplies, with high water requirements after transplantation to

allow for leaf formation, and bulb enlargement. However, control of irrigation is also important to

avoid the formation of persistently humid zones in the field. For these reasons, onion crops are usually

irrigated, using sprinkler, furrow or drip irrigation (Verolet, 2001; LPC bio, 2013; UGA extension,

2014). Irrigation permits the production of less pungent, sweeter, onions (UGA extension, 2014). The


EFSA Journal 2014;12(12):3937 21

relative proportions of the various irrigation techniques and the sources of water in the EU are not

documented. For mature onions, to improve storage ability of the bulb, irrigation is stopped between

1 and 3 weeks before harvest depending on climates and cultivars (Verolet, 2001; UGA extension,

2014). In contrast, for green onions, irrigation just before harvest facilitates pulling out of the plants

from the soil (Chambre d’Agriculture Lot-et-Garonne, 2010).


Onions are particularly demanding of fertilizers to allow adequate development of the aerial part of the

plant as well as the bulb. However, excess or too late supply of nitrogen increases the risk of fungal

disease and reduces storage (Verolet, 2001; LPC bio, 2013; UGA extension, 2014). Organic fertilizers

may be a source of foodborne pathogens if not adequately treated (EFSA BIOHAZ Panel, 2014c).

Manure of various sources can be used but should be applied a few months before sowing or planting

of onions, ideally with a different crop between manure application and onion production (Chambre

d’Agriculture Lot-et-Garonne, 2010; LPC bio, 2013). This represents an approximate delay between

manure application and harvest of 1 year and 8-9 months for mature onions and for green onions,

respectively. Organic fertilizer with rapid nutrient release (e.g. guano) can be used at and after sowing

or planting, but should be stopped at the start of bulb formation (e.g. beginning of July). This could

represent 1 to 3 months delay before harvest for mature onions, but with a shorter delay for green

onions (Verolet, 2001; LPC bio, 2013).

2.3.6. Harvesting

Selection of the harvest date for mature onions is a compromise between yield, quality of the bulb and

storage ability. An optimal harvest time is indicated by a soft neck (attachment of the leaves to the top

of the bulb) and the leaves remaining green. At this stage, the bulbs need post-harvest mechanical

drying. Later harvest provides drier bulbs but with an incompletely closed neck, frequent colonization

by fungal soft rot agents, and with damaged external scales (Chambre d’Agriculture Rhônes-Alpes,

2011; UGA extension, 2014). Bulbs are pulled out, usually mechanically and in dry weather

conditions, then left in the field for 3 to 10 days, depending on the type of onions, for pre-drying

(Chambre d’Agriculture Rhônes-Alpes, 2011; UGA extension, 2014).

For green onions with bulbs (as well as scallions or welsh onions), the harvest should begin when

bulbs are 2-4 cm in diameter, although green onions are also sold without formed bulbs and with only

a white ‘shank’ at the base of the leaves (Civam Bio des Pyrénées-Orientales). Onions are pulled out

usually manually, sometimes with the help of an undercutting tool (NC State University, 2001; Civam

Bio des Pyrénées-Orientales). In the packing house, the outer skin of the onions is removed and

bunches are formed, frequently mechanically (Civam Bio des Pyrénées-Orientales). Leaves are

trimmed to approximately 30 cm length, bunches are washed to remove earth attached on the roots and

packed in boxes (Civam Bio des Pyrénées-Orientales). Washing water can be cooled to rapidly

remove ambient heat from the onions (Oregon State University, 2002a). Bunching onions in the field

is also carried out (Oregon State University, 2002a).


Mature onions must be dried after harvest and before storage to complete drying in the field. Ideally,

bulbs should be dried by forced air at 25-30 °C, 65-80 % RH and for 4-6 days once the batch of bulbs

has reached the target temperature (Chambre d’Agriculture Rhônes-Alpes, 2011) or by forced air at

35-57 °C, 50-65 % RH during 1-2 days (UGA extension, 2014). Drying is completed by intermittent

ventilation for 2-3 weeks at 18-20 °C. The purpose of drying, also called “curing”, is not to dehydrate

the whole bulb but rather to permit healing of any wounds caused by harvest, to allow complete

formation of the layer of dry scales that protect the fleshy scales forming the bulb and to rapidly dry

the neck and the remaining roots before soft rot agents can reach the bulb (Chambre d’Agriculture

Rhônes-Alpes, 2011; UGA extension, 2014). For long storage onions (‘long day’ onions harvested at

the end of the summer), cured bulbs can be stored for up to 6 months in cool (4-8 °C), dry (70-75 %

RH) and well ventilated conditions which avoid any risk of condensation on the bulbs (Chambre


EFSA Journal 2014;12(12):3937 22

d’Agriculture Rhônes-Alpes, 2011), or for about 9 months in cold rooms (-1 to +1 °C) at 70-75 % RH

(Chambre d’Agriculture Rhônes-Alpes, 2011). Controlled atmosphere storage under 3 % oxygen is

also used (UGA extension, 2014). For “short day” onions, which cannot be stored for a long time, cold

rooms (1 °C) can permit storage for one month (UGA extension, 2014). Cold storage breaks dormancy

and induces sprouting of the onion bulbs. To avoid this, chemicals can be applied on the crop before

harvest (see for instance current usage registry in France - Ministère de l'agriculture et de

l'agroalimentaire (online)).

Green onions are perishable; the leaves must remain green, turgid and are particularly susceptible to

moisture loss. Green onions can be stored for 3 to 4 weeks at close to 0 °C and 95 to 100 % RH. At

10 °C, the storage life of green onions is only about 1 week (Oregon State University, 2002a).

In conclusion, harvest and storage differ totally in their objectives for mature onions and for green

onions:

For mature onions, a dry atmosphere is maintained to accelerate healing (curing) of the bulb

tissues and to avoid any ingress of post-harvest plant disease agents. The impact of this curing

step on foodborne pathogens is not known, but the dry environment would presumably not be

favourable to multiplication of Salmonella.

For green onions, harvest and storage conditions are more similar to those of leafy greens,

with the need to maintain high moisture content. Concerning the fate of foodborne pathogens,

green onions are presumably more similar to leafy greens than to mature onions.

2.4. Description of production systems: garlic


Garlic plants do not form true seeds and are always grown from the bulbs (“cloves”), directly planted

in the soil, sometimes in soil covered by plastic lining (Chambre d’Agriculture de la Haute-Garonne,

2004; OMAFRA, 2009). Garlic cloves are planted in autumn from September to November,

depending on cultivars, and harvested from May to September (Appendix A, Freshfel information).


Garlic is normally cultivated in open fields. Soil requirement and soil preparation is similar to that

described for open field onions, with the need of a light soil to permit normal bulb growth, that retain

sufficient humidity and good drainage to avoid stagnation of water. Practices to reduce the risk of

weeds are also similar for garlic as described for onions.


As for onions, garlic is very sensitive to water stress, particularly during foliage development and bulb

growth, but excess water during bulb maturation cause bulb damage. Irrigation is necessary if rain is

not sufficient during these periods, but must be stopped during the last weeks before harvest (Chambre

d’Agriculture de la Haute-Garonne, 2004). Conversely, in more rainy climates, garlic can be planted

on raised beds to increase water drainage (Argouarch'H, 2005). Drip and sprinkle irrigation can be

used, although the major irrigation system is sprinkle irrigation.


As in the case for onions, excess nitrogen for garlic is detrimental to bulb formation. Concerning

organic fertilizers, well-matured compost before plantation is recommended, fresh manure being

unfavourable to garlic crops (Chambre d’Agriculture de la Haute-Garonne, 2004; Argouarch'H, 2005).


EFSA Journal 2014;12(12):3937 23

2.4.5. Harvesting

Garlic bulbs intended to be stored are harvested at a stage which is a compromise between yield and

bulb quality. Harvesting too late produces damaged bulbs while harvesting too early produces bulbs

too rich in water that will shrink during storage (OMAFRA, 2009). A small proportion (around 5 % of

the French garlic production) are consumed “fresh” and can be harvested slightly earlier, for instance

at the end of May-early June instead of mid-June or July for stored garlic (Larousse Agricole, 2002).

However, unlike green onions, “fresh” garlic has a fully formed bulb and leaves are not usually

consumed.

Garlic bulbs can be harvested manually or mechanically. In Italy, around 70 % of the production is

harvested manually but this proportion may vary in other regions. In both cases, bulbs are lifted by a

spade and pulled out. Leaves can be cut at harvest or used to braid several bulbs together. Once

harvested, garlic is peeled to remove only the most external layers. Peeling can be done manually or

mechanically. In most cases, peeling is done manually for optimal quality. However, between 5 and

10 % of the garlic is peeled mechanically. Water is never used in this process.


After harvest, garlic bulbs must be ‘cured’ as described for onion bulbs and with the same purpose.

This can be done by natural ventilation or ideally by forced air at 30 °C. Curing is considered

completed when bulbs have lost 20-25 % of their weight (Chambre d’Agriculture de la Haute-

Garonne, 2004). Once cured, garlic bulbs can be stored at ambient temperature in dry environments

(50-60 % HR) for 4 months (autumn cultivars) or 8 months (spring cultivars). Commercial garlic is

usually stored under controlled temperature. At cold temperature, usually as near as possible to 0 °C

and 50-60 % RH, storage can be increased by up to 6 months for autumn cultivars and by up to

12 months for some spring cultivars stored at -2.5 °C (OMAFRA, 2009) (Appendix A, Freshfel

information). Fresh garlic is sold directly after harvest without curing.

2.5. Description of production systems: celery


Celery seeds are very small and germination is difficult. Celery crops are usually obtained from small

plants produced from seeds at 20-22 °C over 7-8 weeks in nurseries. Planting of seedlings in soil balls

is done in May-June with a harvest in mid-September-October (Argouarch'H, 2005; Chambre

d’Agriculture Bouches-du-Rhône, 2013; Civam Bio Gironde). For some cultivars, coated seeds permit

direct sowing (Civam Bio des Pyrénées-Orientales, 2008b). Celery is very sensitive to competition

from weeds. The same mechanical and thermal techniques, as described for onions, can be used for

celery as well.


Celery grows best in deep, well-drained soils rich in organic matter. To limit weed growth, planting

can be done on soil covered with micro perforated plastic lining to permit homogeneous water

distribution in the soil whenever sprinkler irrigation is used (Civam Bio des Pyrénées-Orientales,

2008b).

For blanching, petioles are progressively covered with soil as they grow, taking care not to cover the

central bud of the plant. Approximately three weeks before harvest, to complete blanching, the whole

plant is covered with soil or a tarpaulin to exclude the light (Argouarch'H, 2005). Alternatively

blanching can be completed after harvest (see Section 2.5.7).

2.5.3. Greenhouse production

Protected culture is done with a different production calendar. Small plants are produced from seeds in

a nursery over 7-8 weeks. In unheated protected culture (in greenhouses or plastic tunnels) in a

Mediterranean climate for instance, for a winter production, planting of small plants in soil balls is


EFSA Journal 2014;12(12):3937 24

done in mid-August, with a harvest in November-December. For a spring production, planting occurs

in March-April for a harvest in May-June (Chambre d’Agriculture Bouches-du-Rhône, 2013). Heated

greenhouses permit planting in autumn and harvest in winter (Civam Bio Gironde).


Irrigation is almost always necessary as celery requires an abundant and regular supply of water

(Argouarch'H, 2005). In particular, water stress may cause flower formation, which hardens the

petioles (Civam Bio Gironde) and results in physiological disorders such as spongy petiole base

(University California, 2008). Irrigation techniques used should permit the rapid saturation of soil

when needed (University California, 2008). Keeping foliage wet increases the risk of fungal diseases

(Civam Bio des Pyrénées-Orientales, 2008b), and drip irrigation can reduce this risk (Oregon State

University, 2002b). However, no information was found on the proportions of irrigation techniques

and water sources used in EU.

2.5.5. Different types of fertilization, organic/manure/compost

Celery requires significant fertilizer input. A high soil organic matter content being favourable to

celery, applying manure is recommended, at e.g. 30 t/ha (Argouarch'H, 2005). However, it should be

very well composted to avoid unbalanced nutrition of the celery plant (Argouarch'H, 2005). Other

organic fertilizer use includes various commercial compost or green manure (Argouarch'H, 2005).

Organic fertilizers should be applied in autumn (Argouarch'H, 2005), which represent, for an open

field production, a delay of nearly one year between manure application and harvest.

2.5.6. Harvesting

For harvest, the whole celery plant is either manually or mechanically lifted from the soil with a blade.

Roots may be cut in the field or left on the celery plant depending on the post-harvest techniques

(Argouarch'H, 2005).

2.5.7. Cooling, post-harvest storage

Celery plants with their roots can be stored in a soil bed in a cool and dark place for 1-2 months, which

will also complete blanching of the petioles (Argouarch'H, 2005). Celery plants without their roots can

be placed in boxes, after trimming damaged leaves, and stored in cold rooms at 2-3 °C for 1-2 months

(Argouarch'H, 2005). Rapid cooling before storage is recommended (Oregon State University, 2002b),

however no information was found on pre-cooling practices in EU for celery. During cold storage,

celery plants are very sensitive to wilting. High humidity should be maintained, either by protecting

boxes with perforated polyethylene films or by maintaining high relative humidity in the cold room

(Oregon State University, 2002b).

2.6. Description of EU bulb and stem vegetables and carrots sector

This Section is based on information provided by Freshfel in July 2013 and August 2014 (Appendix A

and B which present data on volumes of production and trade for the major bulb and stem vegetables

considered in this opinion). Bulb and stem vegetables and carrots on the EU market are predominantly

produced in the EU and the share of imports from third countries is limited. The main EU producing

countries for bulb vegetables are France, Germany and Italy, while third countries supply ca. 5 % of

onions (New Zealand, Egypt, Australia, Chile) and ca. 22 % of garlic (China, Argentina). The main

EU producing countries for stem vegetables are Belgium, France and Germany, while third countries

supply less than 1 % with the exception of asparagus (12 %, mainly Peru). The main EU producing

countries for carrots are Poland, the United Kingdom and Germany, while third countries (Israel,

Turkey) supply only 1.7 %.

The most important bulb and stem vegetables and carrots produced are as follows: onions (ca.

6 million metric tons), carrots (ca. 5.5 million metric tons), leeks (ca. 850 000 metric tons), celeriac

(ca. 350 000 metric tons), shallots (295 000 metric tons) garlic (ca. 280 000 metric tons), asparagus


EFSA Journal 2014;12(12):3937 25

(ca. 170 000 metric tons), kohlrabi (ca. 110 000 metric tons) and green asparagus (ca. 90 000 metric

tons, mainly Spain and Italy). No detailed figures are available for the other products. As the share of

imports from third countries is limited (except for asparagus and garlic), this overview generally

corresponds with the importance of the product categories on retail sale. Generally, the main volumes

of onions, celeriac and kohlrabi will go to the processing industry, as well as substantial volumes of

asparagus and carrots.

There are no detailed statistics available on the share of production of bulb and stem vegetables and

carrots sold directly or undergoing processing. Based on more detailed information per cultivar, about

one third of the carrot acreage is destined for the processing industry. With regard to onions, about

10 % of the supply in the Netherlands is destined for the processing industry.

3. Risk factors for microbiological contamination during agricultural production

Production practices, growth conditions and contact during growth of the outside vegetable surface

with the environment, particularly soil, in combination with intrinsic, extrinsic, harvesting and

minimal processing factors will affect the microbial status of bulb and stem vegetables as well as

carrots at the time of consumption in a similar way to that outlined for leafy greens and melons (EFSA

BIOHAZ Panel, 2014c, e) albeit with different water requirement. Water requirements for the total

melon growing period for a 100-day crop range from 400 to 600 mm, while the water requirements for

lettuce vary from 200 to 400 mm, depending on the climate. In comparison, the water requirements for

the total celery growing period for a 100-day crop is around 400-500 mm (Oregon State University,

2002b); water requirement for green onions varies from 300 – 400 mm, depending on the climate, for

a growing cycle of 60-70 days (Oregon State University, 2002a); for mature onions and garlic water

requirements vary during the production period, with a peak demand during bulb growth of around

50 mm per week, 12-25 mm per week in other periods, and no irrigation a few weeks before harvest

(OMAFRA, 2009; UGA extension, 2014). In addition to the total amount of water used for irrigation,

the need for water shortly before, at harvest, and during post-harvest, is presumably more important

for the presence and survival of micro-organisms. Green onions and celery need water up to harvest

and high humidity post-harvest, in contrast to mature onion and garlic that need dry conditions at these

stages. It has been established that water requirements for carrot production are around 20-25 mm per

week during the growing season, whereas under warm, dry conditions this may increase to 50 mm

(CALU, 2007).

The variability in the production systems and associated environments for production of bulb and stem

vegetables, as well as carrots can lead to a wide range of unintentional or intentional inputs that are

potential sources of food safety hazards. The sources of contamination will vary considerably from

one type of crop production to another as well as between one particular setting/context to another,

even for the same crop. The following Sections are intended to identify and characterize potential risk

factors for contamination of bulb and stem vegetables as well as carrots in addition to those previously

outlined for leafy greens (EFSA BIOHAZ Panel, 2014c) but may not be supported by epidemiological

or experimental evidence, unless specified in the relevant following Sections.

There is limited or no information available on the risk factors for Salmonella, Yersinia, Shigella or

Norovirus in these products during primary production; however, when consumed as ready-to-eat or

minimally processed products, these vegetables are normally not subjected to physical interventions

that will eliminate the occurrence of these pathogens.

3.1. Environmental factors

As with leafy green vegetables (EFSA BIOHAZ Panel, 2014c), environmental factors refer to the

specific conditions of the primary production area, climate and type of crop. These factors may have

an impact on the safety of bulb and stem vegetables as well as carrots, on microbial contamination

routes, persistence of pathogens in fields, the use of fertilizers, sources, quality and frequency of

irrigation water and other water uses, and pathogen prevalence and concentration. Onions, garlic and

carrots grow in the soil and stem vegetables such as celery have prolonged direct contact with soil


EFSA Journal 2014;12(12):3937 26

during growth and/or harvesting, particularly when celery is blanched. In addition, bird faeces and

airborne contaminants (birds nesting around the growth and packing area, nearby livestock or poultry

production, or manure storage or treatment facilities, etc.), and proximity to other wildlife may also

pose a risk of contamination. Whether these vegetables are produced in open fields, in protected

cultivation, or in soil, all impact the environmental risk factors. Each farm environment (including

open field or greenhouse production) should be evaluated independently, as it represents a unique

combination of numerous characteristics that can influence occurrence and persistence of pathogens in

or near bulb and stem vegetable and carrot growing areas.

3.1.1. Factors linked to the adherence, survival and internalisation of pathogens with bulb

and stem vegetables and carrots

Bulb and stem vegetables as well as carrots have smooth surfaces. For some of these vegetables, e.g.

carrots, onion, garlic, the edible portions have extensive and direct contact with soil but have outer

layers which are generally removed before consumption, and for other bulb and stem vegetables, e.g.

spring onions, leeks, celery, the edible portions grow above or near the surface of the ground but are

liable to soil contamination especially during heavy rain and during irrigation.

Difficulties in interpreting data on the interactions and internalisation of pathogens into leafy greens

were previously discussed (EFSA BIOHAZ Panel, 2014c), and despite the very limited data available,

this is equally applicable to bulb and stem vegetables as well as to carrots. A cocktail of 104 cfu of

Salmonella enterica (Basildon, Casbana, Enteritidis, Havana, Mbandaka Newport, Poona and

Schwarzengrund) added to soil used to sow seeds and grow seedlings showed a high (> 94 %)

recovery from the phylosphere of radishes and turnips which was significantly higher than that for

carrots (ca. 74 %) and lettuce (ca. 60 %) or tomato (ca. 46 %) seedlings (Barak et al., 2008).

Furthermore, Salmonella enterica serovars Newport, St. Paul, Typhimurium and Montevideo were

shown to survive in six week old leek shoots, as well as root and soil samples over a 22 day period,

but were shown to persist in significantly higher numbers in the presence of the mycorrhizal fungus

Glomus intraradices (Gurtler et al., 2013). Although radishes and turnips were previously classified as

a root vegetable and not as a bulb and stem vegetable (EFSA Panel on Biological Hazards (BIOHAZ),

2013a), these plant species are included here to provide more information on interactions between

these pathogens and plants.

In a gnotobiotic system, carrot and radish seeds soaked in solutions containing 102 cfu/ml of S.

Typhimurium (resulting in 3-4 log cfu/g of seeds) and after plant growth for 49 days in hydroponic

solution showed multiplication up to 6 log cfu/g of plant tissue (Jablasone et al., 2005). Salmonella

were detected on the surfaces of these plants with internalised populations of the bacterium within the

radish seedlings (Jablasone et al., 2005). In 4 week old spring onion plants inoculated with 1, 3 and

5 log cfu/plant of S. Typhimurium, internalised bacteria were observed after two days in both the

lower as well as the upper parts of the plant (Ge et al., 2013). The level of internalized Salmonella was

significantly greater in the lower part of the plant, especially when exposed to higher inoculum 5 log

cfu/plant (Ge et al., 2013). There is no similar data for other plants and Salmonella, or other bacterial

foodborne pathogens including Yersinia, Shigella and Norovirus. Internalization has been observed

after artificial inoculation of high levels of Salmonella, making it difficult to assess its importance

under natural conditions.

The possibility that lower eukaryotic organisms (particularly nematode worms) may act as a

temporary reservoir for Salmonella in the soil and increase the dispersal and survival of pathogens in

agricultural environments was discussed in relation to the propagation on leafy greens (EFSA

BIOHAZ Panel, 2014c). The same effects are applicable to bulb and stem vegetables as well as carrot

production. Kenney et al. (2006) demonstrated the potential of the nematode Caenorhabditis elegans

to serve as a vector for the transport of S. Newport to the surface of carrots present in soil with bovine

manure. It is not known, however, if similar effects occur for other bulb and stem vegetables as well as

for other pathogens including Yersinia, Shigella or Norovirus.


EFSA Journal 2014;12(12):3937 27

The capacity for Human Norovirus to persist in an infectious state on the surface of bulb and stem

vegetables as well as carrots is not known, due to the inability to culture the virus. No information is

available on the potential for Norovirus to internalise within these vegetables. However, internalisation

of surrogate viruses has been observed in experimental studies. Murine Norovirus can be internalised

in green onion tissues after the plants were grown in hydroponic systems in which a nutrient medium

was inoculated with several logs infectious units of the virus (Hirneisen and Kniel, 2013a): the virus

remained infectious for at least 5 days after internalisation, with no decline in infectivity. No

internalisation was observed in green onion plants grown up to 20 days in soil when the virus was

inoculated into soil substrate, possibly due to adsorption by particulate matter hindering root uptake.

These results do nonetheless demonstrate the possibility that viruses may become located in bulb

tissue e.g. following exposure through irrigation water. However, the virus levels used in experimental

studies may be higher than those which are likely to be encountered during crop production;

furthermore, information on Norovirus internalisation gained through use of surrogates should be

interpreted with caution, as properties of different viruses may affect uptake into, or clearance from,

plants.

3.1.2. Conditions in the field and adjacent land

The conditions in the growing field as well as in adjacent land were identified as playing a vital role in

the microbial safety of leafy greens (EFSA BIOHAZ Panel, 2014c) and these risk factors are likely to

be equally applicable to bulb and stem vegetables as well as carrots. Risk factors for contamination

with pathogens include contact of these vegetables with airborne contaminants as well as those from

the soil, animal droppings, soil amendments (including natural fertilizers) or direct contact with

irrigation water. Risks are consequently associated with runoff and flooding particularly where

adjacent land use is associated with contamination from human or animal excreta. In greenhouse-

grown crops, risks are reduced when contact with the soil is minimized.

3.1.3. Climatic conditions

The effects of climatic conditions on the contamination sources and pathways for pathogens to

contaminate leafy greens during the pre-harvest phase were previously outlined (EFSA BIOHAZ

Panel, 2014c) and risk factors previously identified are also applicable to bulb and stem vegetables as

well as carrots. Heavy rains may increase the exposure to pathogens through contaminated soil, as

well as causing contamination through flooding and where floodwaters come into direct contact with

the vegetables.

3.1.4. Contact with animal reservoirs

Domestic animals (cattle, sheep, chickens, pigs, dogs, cats, and horses) as well as wild animals (e.g.

frogs, lizards, snakes, rodents, foxes, deer, badgers or wild boar) and birds can contaminate leafy

green crops with their faeces if they are present in growing areas (EFSA BIOHAZ Panel, 2014c) and

risk factors previously identified are likely applicable to bulb and stem vegetables as well as carrots.

Bulb and stem vegetables as well as carrots can have high sugar content and are attractive to various

pests including free-living nematodes that may cross-contaminate the vegetables (see Section 3.1.1).

While domestic animals may be separated from growing operations for these vegetables, it can be

more difficult to control access by wild animals and birds. Wild and domestic animal species (as well

as humans) represent risk factors for contamination of these vegetables with pathogens when they are

present in the production environment, and present a risk both from direct contamination of the crop

and soil as well as from contamination of surface water sources and other (particularly water) inputs.

Bird droppings and airborne contaminants (birds nesting around the packing area, nearby livestock,

poultry areas or manure storage or treatment facilities, etc.) may also pose a risk of contaminating

these vegetables with pathogens. In the 2004 outbreak of Y. pseudotuberculosis outbreak in Finland,

the implicated strain was recovered from a pooled sample of the intestinal contents of the common

shrew (Sorex araneus) collected from one of two farms where the carrots were grown (Kangas et al.,

2008).


EFSA Journal 2014;12(12):3937 28

3.2. Organic amendments (manure, slurries, composts, wastewater treatment, sludge and

sewage)

The use of untreated manure and liquid manure are risk factors for contamination of bulb and stem

vegetables as well as carrots. The persistence of foodborne pathogens has been highlighted previously

for leafy greens (EFSA BIOHAZ Panel, 2014c) and depending on length of the production cycle,

these vegetables can be contaminated by pathogens from organic amendments used during cultivation.

Islam et al. (2004) reported that S. Typhimurium survived in soil containing compost for up to

231 days and was detected for 84 and 203 days on radishes and carrots sown into this soil. Similarly,

Natvig et al. (2002) also demonstrated the survival of S. Typhimurium in contaminated manure for at

least 15 weeks in some soils and on growing carrot and radish plants. Greater Salmonella survival was

detected if manure application was carried out in the summer (daily average temperature > 20 °C) than

in the spring (daily average temperature < 10 °C; (Natvig et al., 2002). There is no information on the

survival and persistence of Yersinia, Shigella or Norovirus in similar systems. Section 2 of this

opinion gives some indications on the times organic fertilizers are applied on some bulb and stem

vegetables as well as carrots. As discussed for leafy greens (EFSA BIOHAZ Panel, 2014c),

composting manure may reduce non-spore forming bacterial foodborne pathogens by several logs.

Section 2 of this opinion shows that, to fertilize bulb and stem vegetables, composted manure is also

preferred to raw manure for agricultural reasons.

3.3. Water use during production (irrigation, pesticides and fertilizers, washing)

Clean water should only be used for bulb and stem vegetable production as well as for carrot

production and, as with leafy greens (EFSA BIOHAZ Panel, 2014c): water from contaminated sources

represents a major risk factor for contamination with pathogens. Risks can be minimised by growers

identifying the sources of water used on the farm (e.g. municipal water, reclaimed wastewater,

discharge water from aquaculture, well water, open canal, reservoir, rivers, lakes, farm ponds, etc.).

The risks posed by water should be minimised by assessing the microbial quality of the sources of

water used on the farm for the presence of pathogens which should include documented checks

detailing the potential for microbial contamination from all possible human and/or animal faecal

sources of contamination (e.g. from animals, human habitation, leaks from in-field sanitary facilities,

sewage treatment, manure and composting operations) and the water’s suitability for its intended use.

In the case of identified contamination sources of the water used on the farm, corrective actions should

be taken to minimize the risk. The effectiveness of corrective actions should be verified.

There is evidence that associates irrigation water quality as an important risk for pre-harvest

contamination of radishes and carrots by S. Typhimurium for up to 84 days (Islam et al., 2004). The

risk of sewage or wastewater contaminating vegetables with human foodborne pathogens, including

Salmonella, has been reviewed (Bryan, 1977) although there is no specific information on the survival

and persistence of Yersinia, Shigella or Norovirus associated with the growth of bulb and stem

vegetables as well as carrots. However, it is clear that a wide range of pathogens can occur and persist

in water, as well as surviving in agrichemical solutions, including pesticides. The application of

aqueous fertilizers and pesticides prior to and during harvest may represent a risk if water is

contaminated with pathogens when used in water-based chemical treatments (PMA, 2013).

Water can also be used during post-harvest handling and washing which, if done correctly, may reduce

microbial loads on the outside surface of these vegetables; however, this may also act as a source of

cross-contamination. Although there is no specific information available on the effects of post-harvest

washing for Yersinia, Shigella or Norovirus, some reduction, but not elimination, of S. Typhimurium

was detected in washed radish, although the bacterium was also detected in the wash water that

represents a risk of cross-contamination for subsequently washed vegetables (Natvig et al., 2002).

Water used for post-harvest cooling may also be a significant source of microbial cross-contamination

if this is of poor quality or where there is insufficient disinfectant present. Wet surfaces from cooling

operations or from dew may permit survival and, in some instances, multiplication of human

pathogens on vegetable surfaces.


EFSA Journal 2014;12(12):3937 29

3.4. Equipment

Risks associated with contamination from equipment and handling were previously outlined for leafy

greens (EFSA BIOHAZ Panel, 2014c), which can occur at any point in the farm-to-plate continuum,

and these risk are equally applicable to bulb and stem vegetable production as well as to carrots.

Harvest equipment (knives, pruners, machetes and other cutting equipment), together with transport

containers and any farm machinery (gondolas, trailers or wagons), which comes into contact with

these types of vegetables, represents a risk factor for contamination. Some bulb and stem vegetables

(e.g. green onions, celery, carrots) are typically cooled by forced-air, chilled water, or by use of a

chilled room. Forced-air and hydro-cooling operations may also spread product contamination if

forced air cooling equipment and cooling water is not cleaned and sanitized regularly (PMA and

UFFVA, 2005). In a Y. pseudotuberculosis outbreak linked to grated carrots in Finland, the

investigators noted that storage facilities were open to access by rodents (Jalava et al., 2006).

Mature onions bulbs and garlic are cured by dry warm air. The risk of spreading foodborne pathogens

is not known.

3.5. Worker health and hygiene, worker training

The risk represented by people working with bulb and stem vegetables as well as carrots by the

transfer of micro-organisms of public health concern through direct contact is similar to that

previously considered for leafy greens eaten raw as salads (EFSA BIOHAZ Panel, 2014c). Based on

information provided by Freshfel in June 2015, it should be noted that, in contrast to many other foods

of non-animal origin such as leafy greens, berries, tomatoes or melons, carrots and bulb and stem

vegetables are not usually harvested manually although in some regions these vegetables can be

handled extensively during harvest and during further sorting and packing (Appendix A, Freshfel

information). Thus, as for all other foods of non-animal origin, personal hygiene is critical as manual

harvesting and subsequent handling could lead to contamination. The health and hygiene of harvesters

and other food handlers are critical factors in pathogen contamination, and failure to adhere to

scrupulous hand hygiene is one of the major risk factors. Therefore, improper, careless and poor

handling both in the field and at packing stations (together with inadequate sanitary and hand washing

facilities) can be detrimental, not only for vegetable quality but also for vegetable safety. However,

types of bulb and stem vegetables do not require the same amount of handling, with, for example,

green onions receiving more handling at harvest and post-harvest than mature onions and garlic. In

addition, an inedible skin protects mature onions and garlic, which does not occur for other vegetables

such as green onions and celery.

3.6. Conclusions

The risk factors at primary production for the contamination of bulb and stem vegetables as well as

carrots with Salmonella, Yersinia, Shigella and Norovirus are poorly documented in the literature, with

limited available data but are likely to include the following, based on what is known for other

pathogens or other fresh produce:

environmental factors, in particular proximity to animal-rearing operations and climatic

conditions that increase the transfer to pathogens from their reservoirs to the bulb and stem

vegetables and carrot growing areas;

animal reservoirs (domestic or wild life) gaining access to growing areas for bulb and stem

vegetables or carrots;

contamination or cross-contamination by equipment at harvest or post-harvest, and by

manipulation by workers if this takes place at primary production;

use of untreated or insufficiently treated organic amendments;


EFSA Journal 2014;12(12):3937 30

use of contaminated agricultural water either for irrigation or for application of agricultural

chemicals such as pesticides.

Processes at primary production, which wet the external portions of the crop close to harvest, represent

the highest risk and these include spraying prior to harvest, direct application of fungicides and other

agricultural chemicals and overhead irrigation.

4. Description of minimal processing methods for bulb and stem vegetables and carrots


products, and these steps include selection, washing, cleaning, cutting, packaging and storage. Other

types of minimal processing (e.g. commercial unpasteurized juicing etc.) rarely occur outside retail

and catering, and are not further considered in this Section. Unpasteurized juicing may take place at

retail or catering (especially for carrots) and is considered in Section 6. Freezing may take place, but

this will typically involve a heat blanching process and is outside the scope of this opinion, although

frozen sliced onion may not be blanched (Baert et al., 2008). Bulb and stem vegetables as well as

carrots may be subject to cooking, drying, bottling, canning and other processes, but these are also

outside the scope of this opinion.

As with leafy greens (EFSA BIOHAZ Panel, 2014c), if a washing process is applied during minimal

processing, the quality of the water used for washing bulb and stem vegetables as well as carrots is a

key consideration. Where these vegetables are washed, there will be some effect by reducing the

microbiota (including pathogens) but it may also result in cross-contamination if the microbial quality

of the process water is not controlled using a disinfectant treatment. Thus, the main goal of using

disinfection agents will be to prevent cross-contamination between different batches of vegetables. As

for leafy greens (EFSA BIOHAZ Panel, 2014c), chlorine-derived compounds are the most frequently

used disinfectants during washing in commercial facilities to maintain the quality of the water,

depending upon national policies for their use and approval for the use of disinfectants. The required

free chlorine doses applied to the washing tank will vary depending on the concentration of organic

matter in the process water, although a residual concentration of at least 10-20 ppm of free chlorine is

recommended. In addition, other treatments (e.g. chlorine dioxide, peroxyacetic acid, hydrogen

peroxide, electrolyzed water) have been used on a more experimental basis and are further discussed

in Sections 9.3 and 9.4. Whenever disinfectants are used, the last stage before packaging should be the

rinsing step, which requires very low doses of disinfection agent to maintain the hygienic quality of

the water.

Based on their behaviour in other vegetable food matrices, survival of Salmonella, Yersinia and

Shigella is likely to occur on both ambient-stored as well as refrigerated bulb and stem vegetables as

well as carrots, although there have been limited studies to support this for the specific food types.

Amongst foodborne pathogens considered here, Yersinia enterocolitica and Y. pseudotuberculosis are

the only psychrotrophic micro-organisms and are able to replicate at temperatures below 7 °C.

Norovirus may be able to persist in an infectious state on these vegetables stored at ambient and at

refrigeration temperatures; however, apart from data obtained during outbreaks, no studies are

available to confirm this.

4.1. Onion (washing, peeling and cutting, shredding, packaging)

Green onions are often marketed after a minimal process that consists of washing, draining, cutting

both the roots remaining after harvest and part or all of the stem plate, leaving the very short and

compacted stem that carries the leaves forming the bulb and on which are attached the roots (Hong et

al., 2000). Although minimal, this process induces several physiological changes in the plant tissue

(Hong et al., 2000; 2004) and represents a potential source of contamination. Minimally processed

green onions can be packaged and sealed to prevent moisture loss and stored refrigerated.

Mature bulbs of onion can be peeled and sold as whole peeled onion, or peeled and cut into slices or

diced (Blanchard et al., 1996; Perez-Gregorio et al., 2011). Sliced or diced onion can be sold as such


EFSA Journal 2014;12(12):3937 31

or mixed with other pre-cut vegetables. Peeling onion for removal of the skin can be done by cutting

combined with mechanical procedures, by compressed air, or by abrasion in a water bath. Various

washing procedures, with and without disinfectant, for onion slices or dices have been used, followed

by draining and packaging under various films or atmospheric conditions (Blanchard et al., 1996;

Perez-Gregorio et al., 2011; Berno et al., 2014), but no information was found on the practices actually

used in the EU.

Onion tissues can release antimicrobial compounds upon cutting or crushing (Lund, 1992). However,

onions are also rich in sugars and with pH 5.0 to 5.8, and diced onion supported a 3 log growth of

aerobic bacteria at 4 °C in one week (Blanchard et al., 1996).

At 4 °C, in an atmosphere containing approximately 10 % CO2, a shelf life of 2 weeks was reported

for diced onions (Blanchard et al., 1996).

4.2. Garlic (washing, peeling, packaging)

Garlic can be minimally processed as peeled garlic and is available at retail sale in EU, including in

Spain and Italy. Cloves must be separated from garlic bulbs prior to peeling. Then, cloves are

mechanically peeled and the clove left whole for optimum freshness. Among peeling machines

available for garlic, some use abrasion in association with water but most use compressed air to

eliminate the outer layers. Park et al. (1998) compared dry and wet peeling of garlic and found that

wet peeling produced cloves with a 10 to 100-fold higher counts of total aerobic bacteria. If dry

peeling is applied, peeled garlic is washed in refrigerated water and dried. If a washing tank is used,

disinfectant agents can be used during washing to maintain the quality of the process wash water. Pre-

peeled garlic gloves are stored under refrigerated temperatures to maintain quality. The following

considerations are important to maintain the quality of fresh peeled garlic: 1) reduce mechanical injury

during the peeling process; 2) storage as near as possible to 0 °C; 3) use of modified atmospheres with

0.5 % O2 and 10 % CO2 to retard discoloration and decay as well as sprout development in fresh

peeled garlic stored at 5-10 °C (Cantwell et al., 2003).

4.3. Celery ( washing, peeling, cutting, packaging)

Celery can be minimally processed to various degrees, cutting off petioles to keep the “heart”, using

petioles to produce celery sticks, or celery slices (University California, 2008). No information was

found on the relative frequency of these different minimal processes applied to these products in the

EU and no description of the processing lines was available. Celery sticks and celery dices are

presumably processed as described for leafy greens, with pre-washing, cutting or slicing, washing or

disinfection, rinsing, draining and packaging (Gomez and Artes, 2005). A shelf life of packaged celery

sticks of 10 days at 4 °C was reported (Gomez and Artes, 2005).

4.4. Carrot (washing, peeling, cutting, packaging)

Carrots can be minimally processed to various degrees. Minimally processing of carrots is usually

done in a different processing plant, separately from the post-harvest handling plant. The product is

first peeled and then washed after removal of the top and the bottom of the carrot. Carrots are peeled

with abrasive peeling or knives. Washing is usually carried out in a washing tank and the water is

refreshed on a regular basis. In some cases, the minimal processing is carried out by the carrot

producers, which sell to fresh-cut companies. The fresh-cut companies get ready-to-eat carrots, and

pack them as final product. Carrots are then sold as an individual product or mixed with other types of

ready-to-eat vegetables (Appendix A, Freshfel information).

Ready-to-eat carrots are usually stored at a maximum temperature of 6 ºC and the shelf-life is usually

six days after minimal processing. Commercial ready-to-eat carrots are not commonly packed under

modified atmosphere packaging (MAP) (Appendix A, Freshfel information).


EFSA Journal 2014;12(12):3937 32

White blush, due to dehydration of cut or abrasion-peeled surfaces, has been a problem on fresh-cut

carrots. Sharp cutting blades and residual free-moisture on the surface of the processed carrots will

significantly delay the development of the disorder (Suslow et al., 2002).

5. Risk factors for microbiological contamination during minimal processing treatments,

including the main minimal processing practices

The surface of intact bulb and stem vegetables as well as carrots can be dry or waxy and the pH, water,

protein and sugar content for carrots and onions as compared with lettuce, melon and tomatoes is

shown in Table 2. However, after minimal processing of bulb and stem vegetables as well as carrots,

the surface properties change and there is an increased risk of bacterial contamination, persistence or

growth of both spoilage organisms and potential pathogens, by breaking the natural exterior barrier of

the produce. In general, survival of foodborne pathogens on produce is significantly enhanced once the

protective epidermal barrier has been broken. However, there are opposing effects both from

inhibition by naturally occurring substances within the plant tissue, and interference from the natural

microbiota, including the reduction in pH by the metabolism of lactobacilli.

A mixture of five Salmonella enterica serovars (Michigan, Montevideo, Enteritidis, Agona and

Gaminara) inoculated onto cut celery in closed containers for up to 7 days declined by approximately

one log at 4 °C, did not change at 12 °C, but increased by approximately 2 log cfu/g at 22 °C

(Vandamm et al., 2013). In grated carrot, a mixture of Salmonella enterica serovars (Typhimurium,

Typhi, Infantis and Concord) incubated over 6 days did not show growth at 7 °C or for 2 days at 7 °C

followed by 4 days at 15 °C. However, Salmonella did increase by approximately 1 log10 where stored

at 15 °C despite an approximate 3 log10 increase in lactic acid bacteria at the higher temperature

(Sant'Ana et al., 2012). Growth of S. Typhi was detected on cut surfaces of carrot stored at 32 oC for

6 hours (Viswanathan and Kaur, 2001). There is therefore limited data for the behaviour of Salmonella

in the specific vegetable food matrices, and no information available for Yersinia, Shigella or

Norovirus.

Table 2: pH, water, protein and sugar content of selected fruit and vegetables(a)

Vegetable pH Water (g/100 g) Protein (g/100 g

fresh weight)

Sugar (g/100 g

fresh weight)

Carrot 4.9-6.3 88.3 0.93 4.5

Onion 5.0-5.8 88.5 0.9 4.3

Lettuce 6.0-6.4 95.6 0.9 1.7

Melon (Cantaloupe) 6.2-6.5 90.2 0.84 7.8

Tomato (ripe) 3.4-4.7 94.5 0.88 2.6

(a): Data from Carlin (2007).

Various in vitro antimicrobial activities active against enteric pathogens from plant extracts have been

detected, especially in garlic (Kim and Kim, 2007; Irkin and Korukluoglu, 2009; Gull et al., 2012),

onion (Bakht et al., 2014) and carrots (Rokbeni et al., 2013). Some antimicrobial compounds are

generated upon cutting or mashing the plant tissues, as in onion and garlic (Lund, 1992; Ahsan et al.,

1996).

5.1. Environmental factors

Environmental factors refer to the specific conditions of the processing area, which might have an

impact on the safety of the bulb and stem vegetables as well as carrots and have been previously

considered for leafy green vegetables (CAC, 2003). The environment of the processing plant may

represent a risk for cross-contamination between products. The production environment is likely to be

refrigerated, which, if the product has not already been refrigerated, should be implemented

immediately after harvesting and would prevent the growth of most pathogenic bacteria.


EFSA Journal 2014;12(12):3937 33

5.2. Water sources (washing and other uses)

Washing, if applied, is an important step in the minimal processing of bulb and stem vegetables as

well as carrots. Risk factors previously identified for leafy greens (EFSA BIOHAZ Panel, 2014c) are

applicable to bulb and stem vegetables and carrots. For Salmonella, Yersinia and Shigella, this risk of

cross-contamination during washing is reduced if disinfectants are properly used within the washing

tank. Maatta et al. (2013) detected Y. enterocolitica by PCR in washed, peeled and grated carrots as

well as process wash water, but were unable to isolate the bacterium from these samples; details on

any sanitation agents used in the water were not provided in this report. The effectiveness of

disinfectants against Norovirus is not fully defined due to the lack of an infectivity assay.

5.3. Equipment

Risks from contamination via process equipment were previously discussed for leafy greens (EFSA

BIOHAZ Panel, 2014c), and will be equally applicable to bulb and stem vegetables as well as carrots.

Equipment in the minimal processing environment such as knives and other cutting equipment used in

post-harvesting, as well as the conveyor belts or utensils used for minimal processing, may act as

vehicles for cross-contamination for these vegetables. In an outbreak of Y. pseudotuberculosis

associated with grated carrots in 2003 in Finland, soil samples that contained carrot residue were

obtained from peeling and washing equipment at the production site and were shown to be

contaminated with Y. pseudotuberculosis strains, which were indistinguishable by PFGE from the

outbreak strains (Jalava et al., 2006; Kangas et al., 2008).

5.4. Worker health and hygiene, worker training

Although minimal processing of carrots and onions and other bulb and stem vegetables involves many

types of equipment, in some regions or for some of these vegetables (e.g. peeling of garlic) minimal

processing may still involve extensive manual handling. As previously discussed for leafy greens

(EFSA BIOHAZ Panel, 2014c), lack of compliance of workers with Good Manufacturing Practices

(GMPs) and Good Hygiene Practices (GHPs) and food safety management systems (including

HACCP) are risk factors for minimal processing of bulb and stem vegetable as well as minimal carrot-

processing. Mitigation options include adequate training as well as hand washing and toilet facilities,

which are further considered in Section 16.2.7.

5.5. Conclusions

During minimal processing, contamination or cross-contamination via equipment, water or food

handlers are likely to be the main risk factors for contamination of bulb and stem vegetables as well as

carrots with Salmonella, Yersinia, Shigella and Norovirus.

There is limited information on the behaviours of Salmonella, Yersinia, Shigella or Norovirus in the

specific vegetable food matrices, but these pathogens are likely to survive on the surfaces of these

vegetables for days to several weeks at both ambient and at refrigeration temperatures.

6. Description of the distribution, retail and catering including domestic and commercial

environments for bulb and stem vegetables and carrots

At retail, bulb and stem vegetables as well as carrots can be sold as whole vegetables displayed in bulk

at ambient temperature, which is common practice for carrots, mature onion bulbs, and garlic, but is

also frequent for other bulb and stem vegetables. These vegetables can also be presented as packaged

products after various degrees of minimal processing and, in such cases, are most often displayed in

cold cabinets. This is the case with pre-peeled garlic, which is usually peeled using compressed air,

washed, packaged under modified atmospheres and stored as near as 0 ºC as possible to maintain

quality. Pre-peeled garlic, also known as garlic cloves, is commonly used as an ingredient to prepare

other foods.

In addition to being sold as whole vegetables, bulb and stem vegetables as well as carrots are also sold

as loose cut and shredded products in salad mixes at both retail and in catering and in salad bars,


EFSA Journal 2014;12(12):3937 34

sometimes allowing for self-selection and service by the consumer. Bulb and stem vegetables and

carrots may also be subject to further types of minimal processing (e.g. cutting, mashing and

repackaging) and, particularly for carrots, are also used for production of unpasteurised juices (often

mixed with other fruits or vegetables) usually for immediate consumption or with very short shelf

lives.

At catering and in domestic environments, bulb and stem vegetables are served as fresh cut products

often mixed with other vegetables or salad products as well as being added as an additional flavouring

to more complex foods such as gazpacho or salsa, or as garnishes such as garlic or onions. Fresh garlic

is also crushed and the juice added to dishes or mixed with other ingredients to prepare pastes and

pestos, used to rub bread. All these examples of preparations involve handling and represent generic

opportunities for cross-contamination.

Washing of the product may take place in a similar manner to that outlined in primary minimal

processing, but is more likely to be in sinks with running potable water used for general food handling.

Hygiene practices for preparation of fresh-cut bulb and stem vegetables during catering in the EU are

very diverse and similar to those described for leafy-greens. For instance, in the UK, Sagoo et al.

(2003) described handling conditions for salad vegetables which included carrots, celery, and onions.

The authors reported that salad vegetables were only displayed at chill temperatures (below 8 °C) in

two thirds of the establishments surveyed; specific serving utensils were used by only one third of

these establishments, while use of bare hands to handle salad was observed in another third.

Contaminated salsa was associated with a salmonellosis outbreak in the USA (Campbell et al., 2001)

and survival and growth of Salmonella was affected by the amount of lemon juice or garlic added

during preparation (Ma et al., 2010). Although the lemon juice (as well as vinegar and other organic

acids) will be effective at reducing and preventing the growth of food poisoning bacteria, including

Salmonella (Sengun and Karapinar, 2004), there was evidence of an independent inhibitory effect of

garlic against Salmonella (Ma et al., 2010).

7. Risk factors for microbiological contamination during distribution, retail and catering

including domestic and commercial environments

Risk factors during distribution, retail and catering for bulb and stem vegetables as well as carrots are

likely to be the same or similar to those for leafy greens (EFSA BIOHAZ Panel, 2014c), although they

are not generally supported by published studies. The primary risk factors are contamination from the

environment (e.g. hygiene of premises and storage rooms), cross-contamination through direct or

indirect contact with contaminated water or equipment or handling by infected persons. The quality of

the raw material purchased by the caterer may be an important risk factor, particularly for vegetables

such as carrots that can be stored for several months in high humidity cold rooms, conditions that

could be favourable to growth of psychrotrophic pathogens such as Y. enterocolitica, particularly in

damaged carrot tissues (Rimhanen-Finne et al., 2009).

7.1. Water sources (washing)

As previously outlined for leafy greens (EFSA BIOHAZ Panel, 2014c), water that has been

contaminated with bacteria and viruses, and is then used in food preparation, can cause contamination

of bulb and stem vegetables as well as carrots. This represents a similar contamination or cross-

contamination risk to that which can occur during minimal processing (see Section 5.2). Baert et al.

(2008) demonstrated, using Murine Norovirus, that the potential exists for viruses in contaminated

water used for washing to be transferred the surfaces of onion bulbs: over 3 log infectious units could

be detected on the onion bulbs after washing in water containing 5 log infectious units. It has been

shown that viruses (including Norovirus) can be transferred from contaminated liquid to the surfaces

of other foods (Gerba and Choi, 2006; Rodriguez-Lazaro et al., 2012). There is no direct experimental

evidence for transfer of bacterial foodborne pathogens to bulb and stem vegetables as well as carrots

by this route, although it has the potential to occur.


EFSA Journal 2014;12(12):3937 35

7.2. Equipment, worker health and hygiene, worker training

Due to the wide diversity of foodstuffs potentially prepared and handled in catering establishments,

bulb and stem vegetables as well as carrots can become contaminated. Contamination or cross-

contamination may occur from food contact surfaces, food handlers or from other foodstuffs including

foods of animal origin and, although well documented with other foods (Bolton et al., 2014), there is

only limited evidence of this for bulb and stem vegetables as well as carrots.

In a simulation of cross-contamination within minimal processing environments and domestic

kitchens, Salmonella was readily transferred from the surfaces of freshly cut celery and carrots to a

variety of ceramic, glass, plastic, and stainless steel surfaces (Jensen et al., 2013). This highlights the

importance of segregation of food contact surfaces, for example between raw meat and ready-to-eat

foods of non-animal origin. The investigation of a Y. enterocolitica outbreak caused by consumption

of grated carrot in Finland found the surface of the storage facilities of the vegetable distributor

contaminated by the outbreak strain (Rimhanen-Finne et al., 2009).

Contamination of leafy greens with both Salmonella and Norovirus through contact with the hands of

infected persons during preparation was previously discussed (EFSA BIOHAZ Panel, 2014c), and

similar risks occur with respect to the contamination of bulb and stem vegetables as well as carrots,

which will also apply to Yersinia and Shigella. Poor hand hygiene (e.g. not washing thoroughly)

following use of toilet facilities prior to handling of foodstuffs is an important and universal risk factor

for contamination of food. Risk factors for bulb and stem vegetables as well as carrots in restaurants

will include the potential for cross-contamination between products and utensils as well as from poor

food handler and consumer hygiene.

Shigella can spread from infected individuals by fingers and thus touched utensils or food contact

surfaces can result in contamination or cross-contamination of food. Binet and Lampel (2013)

reviewing historical literature concluded that S. sonnei can survive for over 3 h on fingers, and for

more than 2 to 28 days at 15 °C and up to 13 days at 37 °C on metal utensils.

There is the possibility for Norovirus contamination from food products to spread via cross-

contamination through contact with minimal processing or preparation surfaces as previously

discussed (EFSA BIOHAZ Panel, 2014c). For example, this could occur through cutting of a

contaminated item followed by using the same utensil to cut uncontaminated items without adequate

cleaning between each steps (Wang et al., 2013a; Shieh et al., 2014).

Stals et al. (2013) demonstrated that Norovirus GII.4 could be transferred from gloves to a stainless

steel surface and from that to foodstuffs, and vice versa. In addition, Tuladhar et al. (2013) showed

that transfer of Human Norovirus from finger pads to foods is possible even after the virus is dried on

the surface of the hands.

7.3. Storage temperature

During distribution, retail, catering and in domestic environment, whole mature onion bulbs and whole

garlic bulbs are usually stored at ambient temperatures. Whole green onion and celery are normally

stored refrigerated and packaged to prevent moisture loss, although they can be displayed at ambient

temperature at retail. Minimally processed onions, garlic, green onion and celery are generally stored

at refrigeration temperatures.

Shigella and Salmonella have a minimum temperature for growth at or above 7 °C. But Yersinia is a

genus of psychrotrophic organisms with the ability for growth at usual refrigeration temperatures

(0-7 °C), the latter being well documented for Y. enterocolitica on a wide range of foods (Robins-

Browne, 2013). The growth of Y. pseudotuberculosis in raw ground beef at temperatures ranging from

0 to 30 °C was also described (Bhaduri and Phillips, 2011). Thus, for example, storage of carrots for

an extended period in high humidity cold rooms might enable Yersinia to multiply and grow.

However, no studies are available quantifying the extent of growth on carrots or other bulb or stem


EFSA Journal 2014;12(12):3937 36

vegetables stored in cold conditions. It should be noted however that Liao (2007) reported

Y. enterocolitica, as well as Salmonella, to show very little growth (< 1 log unit) on unsanitized baby

carrots when incubated for 2 days at 20 °C. But on sanitized carrots (using 200 µg of active chlorine)

the growth of Y. enterocolitica (as well as Salmonella) increased 2 to 3 log units, although the growth

of both pathogens was inhibited when co-inoculated with a natural carrot microbiota. Thus it was

shown that the presence of a high level of native microbiota (≥ 104 cfu/g tissue) on baby carrots

greatly limited the growth of these food borne pathogens. The inhibitory effect of carrots on pathogens

is thought to be, in part, due to the antimicrobial activity of carrot tissue and, in part, due to the

antagonistic action of associated microbiota (Liao, 2007).

7.4. Conclusions

At distribution, retail and catering and in domestic and commercial environments, contamination and

cross-contamination, in particular via direct or indirect contact between raw contaminated food and

bulb and stem vegetables, is a risk factor for Salmonella, Yersinia, Shigella and Norovirus. Cross-

contamination risks can also occur in the salad bar environments.

At distribution, retail, catering and in domestic or commercial environments, infected food handlers

are also risk factors (particularly for Norovirus and Shigella). Contamination can be direct or indirect

via poor hand hygiene or food contact surfaces. These contamination and cross-contamination risks

include salad bar environments.

These pathogens are likely to survive on the surfaces of these vegetables for days to several weeks at

both ambient and at refrigeration temperatures.

8. Pathogen occurrence on bulb and stem vegetables and carrots

8.1. Salmonella

8.1.1. Analytical methods for the detection and enumeration of Salmonella in bulb and stem

vegetables and carrots

As previously outlined (EFSA BIOHAZ Panel, 2014c), methods for detection of Salmonella in

FoNAO are well developed and analytical reference methods standardised and widely adopted across

laboratories testing food, including that for Official Control: EN/ISO standard method 657913

which is

prescribed in Regulation 2073/200514

when analysing pre-cut ready-to-eat fruit and vegetables in the

scope of the verification of compliance with the currently established food safety microbiological

criterion for Salmonella. Alternative methods based on modifications of the ISO method using

alternative enrichment media or isolation media (chromogenic media) or using immunoassays and real

time PCR are also available for rapid detection of Salmonella, and many of these methods have been

ISO 1614015

validated showing performance characteristics equivalent to the EN/ISO standard method

6579 (EFSA BIOHAZ Panel, 2014c).

8.1.2. Data on occurrence and levels of Salmonella on bulb and stem vegetables and carrots

There is no routine or regular monitoring of bulb and stem vegetables or carrots for the presence of

Salmonella in the EU Member States and there are limited data on the occurrence of Salmonella in/on

these vegetables in the peer-reviewed world literature (Table 3). There are limited data available from

studies on the occurrence of Salmonella in/on these vegetables, and some of these studies are small

(e.g. comprising < 20 samples) with a variety of methods and sample sizes hence there are difficulties

in making meaningful comparisons between individual studies and in establishing the

13 EN/ISO 6579:2002. Microbiology of food and animal feeding stuffs - Horizontal method for the detection of Salmonella

spp. International Organization for Standardization, Geneva, Switzerland. 14 Commi ssion Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. OJ L 338,

22.12.2005, p. 1-26. 15 ISO 16140:2003. Microbiology of food and animal feeding stuffs – Protocol for the validation of alternative methods.

International Organization for Standardization, Geneva, Switzerland.


EFSA Journal 2014;12(12):3937 37

representativeness of the data on occurrence of the bacterium to estimate the overall levels of

contamination. The majority of the samples were collected outside the EU. It is not possible to include

occurrence data on contamination of these vegetables by Salmonella within zoonoses monitoring data

(according to the Directive 2003/99/EC)16

since these data are aggregated into broad food categories,

e.g. the single category of vegetables and fruits.

16 Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 on the monitoring of

zoonoses and zoonotic agents, amending Council Decision 90/424/EEC and repealing Council Directive 92/117/EEC. OJ

L 325, 12.12.2003, p. 31-40.


EFSA Journal 2014;12(12):3937 38

Table 3: Occurrence of Salmonella in bulb and stem vegetables and carrots

Sampling place Commodity Sampling

country Detection method

Number

of

samples

analysed

Number

of

positive

samples

% of

positive

samples

95 % CI(a) Sample

size Reference

Retail (distribution

centres and markets)

Scallions and green

onions

Canada Health Canada

Compendium of Analytical

Methods MFHPB-20

173 0

0.0

[0, 1.4]

25 g (Arthur et al., 2007)

Retail supermarkets Grated carrot Spain ISO 6579:2002 18 0

0.0

[0, 12.9]

25 g (Abadias et al., 2008)

Retail farmer’s

markets

Carrots Canada Health Canada MFLP-29 206 0 0.0

[0, 1.2] 25 g (Bohaychuk et al., 2009)

Retail farmer’s

markets

Green onions Canada Health Canada MFLP-29 129 0 0.0

[0, 1.9] 25 g (Bohaychuk et al., 2009)

Retail markets and

street vendors

Green onion Saudi Arabia Rappaport-Vassilidis

enrichment screened by

PCR

6 0 0.0

[0, 33] 25 g (Hassan et al., 2011)

Retail markets and

street vendors

Celery Saudi Arabia Rappaport-Vassilidis

enrichment screened by

PCR

8 0 0.0

[0, 26.2] 25 g (Hassan et al., 2011)

Restaurants Carrot juice Mexico NS 280 24 8.6

[5.7, 12.3]

NS (Torres-Vitela et al., 2013)

Retail markets

Celery

USA NS 12 0 0.0 [0, 18.5] 25 g (Thunberg et al., 2002)

Central produce

supply

Celery Mexico Enrichment in Rappaport-

Vassiliadis broth and

subcultured onto brilliant

green, XLD and

MacConkey’s agars

100 3 3.0 [0.9, 7.8] 50 g (Quiroz-Santiago et al., 2009)

Central produce

supply

Onion Mexico Enrichment in Rappaport-

Vassiliadis broth and

subcultured onto brilliant

green, XLD and

MacConkey’s agars

100 0 0.0 [0, 2.5] 50 g (Quiroz-Santiago et al., 2009)

Markets

Stem and root

vegetables(b)

Spain Tetrathionate-Kauffman

broth subcultured onto SS

agar

204 5 2.5 [0.9, 5.3] NS (Garcia-Villanova Ruiz et al.,

1987)

Wholesale and retail

stores

Celery, carrots,

radish or spinach

USA Official Methods of

Analysis 13th Ed

50(c) 4(c) 8.0 (c)

[2.8, 17.9] NS (Rude et al., 1984)

Retail Celery (organic) UK PHLS (ISO 6579) 193 0 0.0 [0, 1.3] 25 g (Sagoo et al., 2001)


EFSA Journal 2014;12(12):3937 39



Number

of

samples

analysed

Number

of

positive

samples

% of

positive

samples

95 % CI(a) Sample

size Reference

Retail Spring onions

(organic)

UK PHLS (ISO 6579) 87 0 0.0 [0, 2.8] 25 g (Sagoo et al., 2001)

Retail Carrots (organic) UK PHLS (ISO 6579) 478 0 0.0 [0, 0.5] 25 g (Sagoo et al., 2001)

Import Celery USA from

various

countries

NS 84 1

1.2

[0.1, 5.4]

16 oz (US-FDA, 2001)

Street vendors Carrot India FOA, Manual of Food

Quality Control

8 2 25.0 [5.6, 59.2] 25 g (Viswanathan and Kaur, 2001)

Street vendors Celery India FOA, Manual of Food

Quality Control

8 5 25.0 [5.6, 59.2] 25 g (Viswanathan and Kaur, 2001)

NS: not stated

(a): The credible interval was calculated using a Bayesian approach and taking as prior beta (1/2,1/2) (Miconnet et al., 2005).

(b): Garlic, sweet potato, onion, chive, mushroom, turnip, potato, leek, radish, beet and carrot.

(c): One sample of celery, carrot, radish and spinach. Denominators of each vegetable not stated.


EFSA Journal 2014;12(12):3937 40

8.2. Yersinia

8.2.1. Analytical methods for the detection and enumeration of Yersinia in bulb and stem


The genus Yersinia comprises three species, which are potentially pathogenic to humans: Y. pestis,

Y. pseudotuberculosis, and Y. enterocolitica. Of these, Y. enterocolitica is most important as a cause of

foodborne illness and serogroups that predominate in human illness are O:3, O:8, O:9, and O:5,27. Y.

pseudotuberculosis is less ubiquitous than Y. enterocolitica, and although frequently associated with

animals, has only rarely been isolated from soil, water, and foods. Y. pestis is not a foodborne

pathogen: it is transmitted to its host via flea bites or via the respiratory route. Analytical methods for

the detection of presumptive pathogenic Y. enterocolitica in food stuffs have been developed and

adopted across laboratories testing food. The reference method for official controls includes the

EN/ISO standard method 10273:2003.17

The presence of pathogenic Y. enterocolitica is determined

qualitatively by a combination of selective enrichment and subculture on selective agar media. Isolated

presumptive colonies are purified and subsequently subjected to biochemical characterisation

(enabling biotyping) and optional serological confirmation and pathogenicity testing (the mechanisms

of pathogenicity of enteropathogenic Yersinia are complex and include a number of both

chromosomally and plasmid determined factors). The isolation methods used for Y. enterocolitica are

also used for Y. pseudotuberculosis, but are generally insufficient for the latter species as selective

enrichment is inefficient for the recovery of this species (Niskanen et al., 2002; Laukkanen et al.,

2008). As an alternative, real time PCR method for detection of pathogenic Y. enterocolitica and

Y. pseudotuberculosis in food is also available (e.g. NMKL 163).18

8.2.2. Data on occurrence and levels of Yersinia on bulb and stem vegetables and carrots


Yersinia in the EU Member States and there are limited data on the occurrence of Yersinia in/on these

vegetables in the peer-reviewed world literature (Table 4). Since only two studies were located in the

EU there are limited data available from studies on the occurrence of Yersinia in/on these vegetables,

and these studies are small (e.g. comprising < 32 samples). It is not possible to include occurrence data

on the contamination of these vegetables by Yersinia within the zoonoses monitoring data (according

to the Directive 2003/99/EC)19

since these data are aggregated into broad food categories, e.g. the

single category of vegetables and fruits. Consequently, there are difficulties in assessing the

representativeness of these data to estimate the overall levels of contamination.

17 EN/ISO 10273:2003. Microbiology of food and animal feeding stuffs - Horizontal method for the detection of presumptive

pathogenic Yersinia enterocolitica. International Organization for Standardization, Geneva, Switzerland. 18 NMKL 163:2013. Pathogenic Yersinia enterocolitica and Yersinia pseudotuberculosis - real-time PCR methods for

detection in food, feed and environmental samples. 2nd Edition. 19 Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 on the monitoring of zoonoses


12.12.2003, p. 31-40.


EFSA Journal 2014;12(12):3937 41

Table 4: Occurrence of Yersinia. in bulb and stem vegetables and carrots

Sampling

place Commodity

Sampling


Number

of

samples

analysed

Number

of

positive

samples

% of positive samples 95 % CI(a) Sample

size Reference

Retail

supermarkets

Grated carrot Spain ISO 10273:2003 for Yersinia

enterocolitica

18 0 0

(Y. enterocolitica)

[0, 12.9]

25 g (Abadias et al.,

2008)

Minimal

processing

plants

Washed whole, peeled,

cut and grated carrots

Finland ISO 10273:10273 with

modifications

(Y. enterocolitica)

USFDA Bacteriological

Analytical Manual

(Y. pseudotuberculosis)

32 0 0

(Y. pseudotuberculosis)

[0, 7.5]

25 g (Maatta et al.,

2013)

NS: not stated

NA: not applicable



EFSA Journal 2014;12(12):3937 42

8.3. Shigella

8.3.1. Analytical methods for the detection and enumeration of Shigella in bulb and stem


The genus Shigella consists of four species: S. dysenteriae (subgroup A), S. flexneri (subgroup B),

S. boydii (subgroup C), and S. sonnei (subgroup D) all of which cause human disease. S. flexneri and

S. sonnei are most associated with food borne disease. S. boydii is infrequently identified as a

foodborne pathogen. Shigella organisms may be very difficult to distinguish biochemically from

Escherichia coli. As is the case for pathogenic E. coli, the virulence of Shigella is multifactorial,

involving both chromosomal and plasmid genes with the essential role of a large plasmid involved

allowing invasion (Binet and Lampel, 2013). ISO 21567:200420

specifies a horizontal method for the

detection of Shigella species. The presence of Shigella can be determined qualitatively by a

combination of selective enrichment and subculture on multiple selective agar media. Isolated

presumptive colonies are purified and subsequently subjected to biochemical and serological

confirmation. Reliable detection and isolation of Shigella from foods is challenging, due to the

organism being easily overgrown by the competing microbiota (Uyttendaele et al., 2001). As an

alternative, a real time PCR method for detection of Shigella in food is also available (e.g. NMKL

174).21

8.3.2. Data on occurrence and levels of Shigella on bulb and stem vegetables and carrots


Shigella in the EU Member States and there are limited data on the occurrence of Shigella in/on these

vegetables in the peer-reviewed world literature (Table 5). There are limited data available from

studies on the occurrence of Shigella in/on these vegetables, and some of these studies are small (e.g.

comprising < 10 samples) with a variety of methods and sample sizes hence there are difficulties

making meaningful comparisons between individual studies difficult and in establishing the

representativeness of the data on occurrence of the bacterium. All samples were collected outside the

EU. It is not possible to include occurrence data on contamination of these vegetables by Shigella

within zoonoses monitoring data (according to the Directive 2003/99/EC)22

since these data are

aggregated into broad food categories, e.g. the single category of vegetables and fruits.

20 EN/ISO 21567:2004. Microbiology of food and animal feeding stuffs - Horizontal method for the detection of Shigella spp.

International Organization for Standardization, Geneva, Switzerland. 21 NMKL 174:2002. Shigella spp. PCR method for detection in foods. 2nd Edition. 22 Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 on the monitoring of zoonoses


12.12.2003, p. 31-40.


EFSA Journal 2014;12(12):3937 43

Table 5: Occurrence of Shigella in bulb and stem vegetables and carrots



Number

of

samples

analysed

Number

of

positive

samples

% of

positive

samples

95 % CI(a) Sample

size Reference

Retail (distribution

centres and markets)

Organic scallions

and green onions

Canada Health Canada Compendium of

Analytical Methods MFLP-25

173 0 0 [0, 1.4] 25 g (Arthur et al., 2007)

Retail markets and

street vendors

Green onion Saudi Arabia AOAC Compendium of Methods for

Microbiological examination of

Foods 2001

6 0 0 [0, 33] 25 g (Hassan et al., 2011)

Retail markets and

street vendors

Celery Saudi Arabia AOAC Compendium of Methods for

Microbiological examination of

Foods 2001

8 0 0 [0, 26.2] 25 g (Hassan et al., 2011)



EFSA Journal 2014;12(12):3937 44

8.4. Norovirus

8.4.1. Analytical methods for the detection and enumeration of Norovirus in bulb and stem


Information on the standardisation of methods for detection of Norovirus in foods can be found in

Section 4.3.2 of the scientific opinion of the EFSA Panel on Biological Hazards (BIOHAZ) (2011b).

There are two ISO/CEN methods23

which are currently available for Norovirus detection and

quantification, respectively, in food. These methods currently have the status of a Technical

Specification (TS) and, based upon validation data, will need to be reviewed three years after initial

publication before becoming a full International Standard.24

The methods are technically complex, and

their performance strictly according to their technical specifications can only be carried out in

specialised and well-resourced laboratories with skilled personnel. In particular, the production of the

nucleic acid controls is challenging, and the availability of reliable quality control materials and

External Quality Assurance (EQA) schemes will be necessary before there can be complete

confidence in the concordance of results between laboratories. These ISO/CEN methods are currently

technical specifications and have the opportunity to be further refined with regard to sampling, sample

preparation, limit of detection and interpretation of results. To date, there are few reports of analytical

methods for Norovirus detection on bulb and stem vegetables (e.g. onion and garlic) and carrots.

ISO/TS 15216-1 and ISO/TS 15216-2 refer to detection of Norovirus on leafy green vegetables and

berry fruit. However, it should be possible to apply them to the detection of Norovirus on bulb and

stem vegetables and carrots.

8.4.2. Data on occurrence and levels of Norovirus on bulb and stem vegetables and carrots


Norovirus in the EU Member States and there are limited data on the occurrence of Norovirus in/on

these vegetables in the peer-reviewed world literature (Table 6). There are limited data available from

studies on the occurrence of Norovirus in/on these vegetables, and all of these studies are small (e.g.


making meaningful comparisons between individual studies and in establishing the representativeness

of the data on occurrence of the virus. All of the samples were collected outside the EU. It is not

possible to include occurrence data on contamination of these vegetables by Norovirus within

zoonoses monitoring data (according to the Directive 2003/99/EC)25

since these data are aggregated

into broad food categories, e.g. the single category of vegetables and fruits.

23 ISO/TS 15216-1: Microbiology of food and animal feed - Horizontal method for determination of hepatitis A virus and

norovirus in food using real-time RT-PCR - Part 1: Method for quantification. International Organization for

Standardization, Geneva, Switzerland.

ISO/TS 15216-2: Microbiology of food and animal feed - Horizontal method for determination of hepatitis A virus and

norovirus in food using real-time RT-PCR - Part 2: Method for qualitative detection. International Organization for

Standardization, Geneva, Switzerland. 24 International Organization for Standardization. ISO deliverables. ISO/TS technical specification. Available online:

http://www.iso.org/iso/home/standards_development/deliverables-all.htm?type=ts 25 Directive 2003/99/EC of the European Parliament and of the Council of 17 November 2003 on the monitoring of zoonoses


12.12.2003, p. 31-40.

http://www.iso.org/iso/home/standards_development/deliverables-all.htm?type=ts


EFSA Journal 2014;12(12):3937 45

Table 6: Occurrence of Norovirus on bulb and stem vegetables and carrots

Sampling

place Commodity

Sampling

country

Number of

samples

analysed

Number of

samples

where

Norovirus

detected

% of

positive

samples 95 % CI(a) Reference

Farms Green

onions Egypt 144 49 34.0 [26.7 ,42]

(El-Senousy et

al., 2013)

Farms Leek Egypt 144 30 20.8 [14.8, 28] (El-Senousy et

al., 2013)

Market Baby carrot USA 31 3 9.7 [2.8, 23.6] (Groman et al.,

2010)

Market Green

onions USA 21 1 4.7 [0.5, 20.2]

(Groman et al.,

2010)

Market Green

onions Malaysia 30 4 13.3 [4.7, 28.7]

(Noor Hidayah

et al., 2011)

Catering Green

onions Turkey 92 1 1.1

[0.1, 5]

(Yilmaz et al.,

2011)

(a): The credible interval was calculated using a Bayesian approach and taking as prior beta (1/2,1/2) (Miconnet et al.,

2005).

The samples described in Table 6 were analysed in the course of four research surveys, none of which

occurred in the EU. None of the foodstuffs sampled were known to be linked to any outbreaks. The

analyses used methods similar to the standardised methods described in ISO/TS 15216-1 and ISO/TS

15216-2, in general or specific aspects.

Groman et al. (2010) surveyed produce items collected from 14 states in the USA, and found

3/31 baby carrot samples and 1/21 green onion samples to be contaminated with Norovirus GII.

Analysing green onions from salad bars and restaurants in Istanbul, Yilmaz et al. (2011) found one

sample contaminated with Norovirus GII out of the 93 tested. Noor Hidayah et al. (2011) found

4 samples (out of 30 tested) of green onion and one sample (out of 30 tested) of red onion obtained

from a local market in Selangor, Malaysia, to be contaminated with Norovirus GI. El-Senousy et al.

(2013) found 49/144 green onion samples collected from farms in the Nile Delta in Egypt to be

contaminated with a mean of 5.6×101 Norovirus GI, and 30/144 leek samples 37/144 radish samples

from the same sources to be contaminated with a mean of 5.9×101 Norovirus GI. The high prevalence

of Norovirus contamination observed in this latter study was likely due to the water used for irrigation

of the vegetables being drawn from contaminated river sources: the same study found 36/144 (25.0 %)

of irrigation water samples from the farms to be positive for Norovirus GI (El-Senousy et al., 2013).

8.5. Conclusions


Salmonella, Yersinia, Shigella and Norovirus in the EU Member States and there is limited data on the

occurrence of these pathogens in/on these vegetables in Europe. There are limited studies available in

the peer-reviewed world literature on the occurrence of Salmonella, Yersinia, Shigella and Norovirus

on/in bulb and stem vegetables or carrots. Hence, there are difficulties in both making meaningful

comparisons between individual studies as well as assessing the representativeness of these data to

estimate the overall levels of contamination.

9. Mitigation options to reduce the risk to humans posed by Salmonella, Yersinia, Shigella

or Norovirus contamination in bulb and stem vegetables and carrots

9.1. Introduction

Many of the mitigation options previously outlined for leafy greens (EFSA BIOHAZ Panel, 2014c)

are generic and equally applicable to other foods of non-animal origin, including bulb and stem

vegetables as well as carrots. However, there are some differences, inherent to bulb and stem

vegetables as well as carrots, which are substantially different commodities than leafy greens with


EFSA Journal 2014;12(12):3937 46

respect to: (i) the production system (true bulbs and roots are normally formed underground although

some plants such as garlic can also produce aerial small bulbs, or for green (immature) onions also the

leaves can be used for consumption); (ii) often mechanical harvest occurs and thus there is little or no

hand picking; (iii) their intrinsic characteristics (most of these vegetables have a quite robust peel or

external protection against microbial contamination, for some antimicrobial activity has been

described); (iv) a longer shelf life and prolonged stored postharvest is common either dried (e.g.

onions) or kept in soil under humid conditions (carrots), and (v) epidemiological evidence associating

their consumption with foodborne outbreaks is often linked to catering, restaurants or home

consumption where these type of vegetables have been subject to extensive manual handling in

preparation of ready-to-eat fresh-cut or grated raw vegetables in salad bars.

9.2. General mitigation options

Appropriate implementation of food safety management systems including Good Agricultural

practices (GAP), Good Hygienic Practices (GHP) and Good Manufacturing Practices (GMP) should

be the primary objective of operators producing bulb and stem vegetables as well as carrots. These

food safety management systems should be implemented along the farm to fork continuum and should

be applicable to the control of a range of microbiological hazards. Although some intervention

strategies or control measures can be defined to prevent, limit the spread or sometimes reduce the level

of contamination, the main focus for food safety management should be on preventive measures, as it

is difficult to define critical control points (CCPs) that either eliminate the microbial hazard or

significantly reduce it. Codes of practice and guidelines should encourage the use of appropriate good

agricultural and hygiene practices at farm level. Food safety management based upon GMP and

HACCP principles should be the objective of processors, distributors, retailers and caterers involved in

production of bulb and stem vegetables and carrots. In addition, the responsibilities of the food

business operators producing or harvesting plant products require them to take adequate control

measures as outlined in Regulation (EC) No 852/200426

and these are identical to those outlined

previously (EFSA BIOHAZ Panel, 2014c). Where practicable, a comprehensive food safety control

plan that includes a written description of each of the hazards identified in assessing environmental

hygiene and the steps to be implemented to address each hazard should be prepared at primary

production (EFSA BIOHAZ Panel, 2014c), and there should be complete traceability through primary

production, processing, distribution, retail, and catering, up to consumption of all products. Mitigation

options through compliance with existing prerequisite programs such as GAP and GMP, and with

recommended Codes of Practices and guidance such as the relevant Codex guidelines, should assist in

reducing risks of contamination by Salmonella, Shigella, Yersinia and Norovirus.

9.2.1. Environment

As outlined with leafy greens (EFSA BIOHAZ Panel, 2014c), primary production should not be

carried out in growing areas where the known or presumptive presence of pathogens would lead to an

unacceptable likelihood of transfer to horticultural crops intended for human consumption without a

validated process kill step (CAC, 1969, 2003) which includes bulb and stem vegetables as well as

carrots which are eaten raw or minimally processed. Production areas should be evaluated for hazards

that may compromise hygiene and food safety, particularly to identify potential sources of faecal

contamination. If the evaluation concludes that contamination in a specific area is at levels that may

compromise the safety of crops, in the event of heavy rainfall and flooding for example, intervention

strategies should be applied to restrict growers from using this land for production of these vegetables

until the hazards have been addressed. Preventive measures are not always easy to implement as

farmers may not control adjacent land activities, or the land history does not include knowledge of the

level of pathogens in the soil or the time taken to reduce these to acceptable levels (Suslow et al.,

2003; James, 2006; Gil et al., 2015).

26 Regulation (EC) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of

foodstuffs. OJ L 139, 30.4.2004, p.1-54.


EFSA Journal 2014;12(12):3937 47

Bulb and stem vegetables as well as carrots are likely to be in direct contact with soil during growth

and/or harvesting. Bird droppings and airborne contaminants (nearby livestock, poultry areas or

manure storage or treatment facilities, etc.) may also pose a risk of contamination. Domestic and wild

animals should be excluded from production areas, to the extent possible, using appropriate biological,

cultivation, physical and chemical pest control methods.

9.2.2. Manure, sewage and sewage sludge

Appropriate production, storage, management and use of manure or sludge is equally important for

bulb and stem vegetable production as well as carrot production to reduce residual pathogen

populations as outlined for leafy greens (EFSA BIOHAZ Panel, 2014c) and treatment procedures to

reduce or eliminate pathogens from contaminated manure are, as with any ready-to-eat food, equally

applicable. The same consideration for the use of organic amendments previously outlined for leafy

greens (EFSA BIOHAZ Panel, 2014c) also apply to production of these vegetables.

9.2.3. Water

Although, bulb and stem vegetables are usually cultivated with the use of natural rainfall, artificial

irrigation is sometimes used and it is important to select appropriate irrigation sources and avoid, if

possible, uncontrolled sources of water such as rivers and lakes as was previously outlined for leafy

greens (EFSA BIOHAZ Panel, 2014c). Since bulb and stem vegetables can be intended for direct

consumption, for washing (if applicable), clean or potable water is recommended for use. It is

recommended that the quality of the water used in packing establishments be controlled and

monitored, i.e. recording testing for indicator organisms and/or foodborne pathogens and, if necessary,

treated before use.

9.2.3.1. Water in primary production

Risks can be minimised by growers identifying the sources of water used on the farm (municipality,

re-used, irrigation water, reclaimed wastewater, discharge water from aquaculture, well, open canal,

reservoir, rivers, lakes, farm ponds, etc.) and identifying vulnerabilities to faecal contamination.



contaminated by human sewage or faecal wastes from other animals.

Among the potential interventions, both water treatment or efficient drainage systems that take up

excess overflows are needed to prevent the additional dissemination of contaminated water. The risks

posed by water should be minimised by assessing the microbial quality of the sources of water used on

the farm for the presence of pathogens. This should include a documented check detailing the potential

for microbial contamination from all possible human and/or animal faecal sources of contamination

(e.g. from animals, human habitation, leaks from on-field sanitary facilities, promiscuous defecation in

production environments, sewage treatment, manure and composting operations) and the water’s

suitability for its intended use. In the case of identified contamination sources of the water used on the

farm, corrective actions should be taken to minimize the risk of exposure to the carrots, bulb and stem

vegetables. The effectiveness of corrective actions should be verified. Identifying and implementing

corrective actions is a means to prevent or minimize contamination of water for primary production

(e.g. settling or holding ponds that are used for subsequent irrigation and/or harvesting may attract

animals or in other ways increase the microbial risks associated with water for irrigation). Possible

corrective actions may include fencing to prevent large animal contact, proper maintenance of wells,

filtering water, not stirring the sediment when drawing water, building settling or holding ponds, and

water treatment facilities and water treatment. Since E. coli is an indicator micro-organism for faecal

contamination in irrigation water, growers should arrange for periodic testing to be carried out to

inform preventive measures. Additional analytical testing may be necessary after a change in irrigation

water source, flooding or a heavy rainfall when water is at a higher risk of contamination.


EFSA Journal 2014;12(12):3937 48

9.2.3.2. Process wash water

Mitigation strategies aiming to reduce risks of microbial contamination and cross-contamination for all

water used during minimal processing were previously discussed for leafy greens (EFSA BIOHAZ

Panel, 2014c). Potable water should be used during minimal processing and this should include wash-

water where used, as well as that used for hydro-cooling, or other uses. To maintain the microbial

quality of the water and avoiding cross-contamination in a washing tank, the use of disinfectant agents

is recommended. Disinfection solutions should be monitored to ensure that the disinfectant is present

at sufficient levels to achieve its intended purpose reducing the potential for cross-contamination

(without generation of chemical by-products).

Water that is used in hydro-coolers should be of potable quality. Water that is used only once and not

recirculated is preferable. If water is used for cooling and is recirculated, it should be evaluated and

monitored to ensure that disinfectant levels, if used, are sufficient to reduce the potential risk of cross-

contamination (without generation of chemical by-products).

9.2.4. Equipment

The adherence to adequate cleaning and disinfection of equipment used in harvest and postharvest

sorting, packing or further minimal processing is an important preventive measure to avoid microbial

contamination of equipment as was previously outlined for leafy greens (EFSA BIOHAZ Panel,

2014c) and similar considerations apply to bulb and stem vegetables and carrots production and

minimal processing. Growers should ensure that clean pallets and containers (disinfected where

necessary) are used, and take measures to ensure that the containers do not come into contact with

unprocessed manure or other sources of cross-contamination.

If these vegetables pass over brushes in either dry or wet cleaning, care should be taken to ensure they

do not damage or result in cross-contamination, and these brushes should be routinely inspected,

cleaned and adjusted as needed.

Cooling equipment should be cleaned and disinfected on a regular basis according to written

procedures to ensure that the potential for cross-contamination is minimized.

Handling of bulb and stem vegetables may include harvest, transport to packing house, curing and

storage such as the case of onions, washing, sorting and grading, hydro-cooling and packaging

(Garrett et al., 2003). Bulb and stem vegetables and carrots should be washed with potable water

before cutting or peeling (if appropriate to the process), although some, like onions, can be dry peeled.

Cutting or peeling knife blades should be cleaned and disinfected on a regular basis according to

written procedures to reduce the potential for cross-contamination during the cutting or peeling

process.

Before cutting or other minimal processing, a further reduction in microbial contamination may be

achieved by scrubbing in the presence of a sanitizer or application of an alternative surface

decontamination process such as hot water, steam or other treatments. Knife blade disinfection

solutions should be monitored to ensure that the disinfectant is present at sufficient levels to achieve

its intended purpose and does not promote the potential for cross-contamination.

9.2.5. Training and education of workers

The importance of standard enforceable policies and provision of training in sanitation for all

employees working in primary production, minimal processing, retail and catering was emphasised for

leafy greens (EFSA BIOHAZ Panel, 2014c). Compliance with hygiene requirements, in particular

hand hygiene, is an absolute necessity for food handlers at all stages of the production and supply

chain of bulb and stem vegetable as well as carrots to reduce the risks of Salmonella, Shigella and

Norovirus contamination but is also to be taken into consideration for controlling Yersinia. Only

workers who have been trained in hygienic handling should be assigned to pick, pack or process these

vegetables. All persons involved in handling (cutting, grating, dicing, etc.) of bulb and stem vegetables


EFSA Journal 2014;12(12):3937 49

as well as carrots for buffets in catering and restaurants should receive hygiene training appropriate to

their tasks and receive periodic assessment while performing their duties to ensure tasks are being

completed with due regard to good hygiene and hygienic practices.

9.2.6. Final product

Since Salmonella, Shigella, Yersinia and Norovirus are able to survive on intact bulb and stem

vegetable as well as carrots from days to several weeks at both ambient and refrigeration temperatures,

and may grow and penetrate into wounded tissues as well as on cut vegetables, adequate storage

conditions should be applied to these products.

For bulb and stem vegetables and carrots normally stored at ambient temperature in a dry

environment, such as mature bulbs of onions and garlic bulbs, consumers should be aware that cuts,

slices of these vegetables or preparation of these vegetables such as sauces, pastes and pesto may

support growth of foodborne pathogenic bacteria and should be kept refrigerated for no more than a

few days.

Consumers need to be advised on how to handle, prepare, and store bulb and stem vegetables as well

as carrots safely (preferably in a cool environment) and to avoid cross-contamination with foodborne

pathogens from various sources (e.g. hands, sinks, cutting boards, utensils, raw meats). They should

also be given guidance on correct hand washing methods, and the need to properly peel or wash

carrots and bulb and stem vegetables with potable water before consumption.

As bulb and stem vegetables come from soil or have been in close contact with soil, and can be stored

for extended periods before retail sale, consumers should be advised to wash and/or scrub whole or

peeled (whatever appropriate) bulb and stem vegetables as well as carrots using potable running water

and, where appropriate, disinfectant solutions before consumption. Pre-cut products should not be

rewashed. It is recommended that pre-cut carrots and other bulb and stem vegetables should be

wrapped/packaged and refrigerated as soon as possible and distributed and kept under refrigeration

temperatures.

9.2.7. Conclusions

Compliance with existing prerequisite programs such as Good Agricultural Practices (GAP) and Good

Manufacturing Practices (GMP), and with recommended Codes of Practices and guidance such as the

relevant Codex guidelines, will assist Salmonella, Shigella, Yersinia and Norovirus risk mitigation

strategies in primary production.

Production areas should be evaluated for hazards that may compromise hygiene and food safety,

particularly to identify potential sources of faecal contamination. If the evaluation concludes that

contamination in a specific area is at levels that may compromise the safety of crops, in the event of

heavy rainfall and flooding for example, intervention strategies should be applied to restrict growers

from using this land for production of these vegetables until the hazards have been addressed.

Each farm environment (including open field or greenhouse production) should be evaluated

independently as it represents a unique combination of numerous characteristics that can influence

occurrence and persistence of pathogens in or near bulb and stem vegetables as well as carrot growing

areas.



contaminated by sewage.

Both water treatment and efficient drainage systems that take up excess overflows are possible

mitigation options to prevent the additional dissemination of contaminated water. The risks posed by

water should be minimised by assessing the microbial quality of the sources of water used on the farm


EFSA Journal 2014;12(12):3937 50

for the presence of pathogens. Since E. coli is an indicator micro-organism for faecal contamination in

irrigation water, growers should arrange for periodic testing to be carried out to inform preventive

measures. Appropriate production, treatment, storage, management and use of manure or sludge are

important.

During minimal processing GMP and food safety management systems (including HACCP) will assist

Salmonella, Yersinia, Shigella and Norovirus risk mitigation strategies.

It is recommended that water used during minimal processing be monitored to assess its microbial

quality. When disinfectants are used in wash water, the concentration should be monitored to verify

that they are applied effectively to reduce the potential risk of cross-contamination while avoiding the

accumulation of disinfection by-products.

Furthermore, the main mitigation options for reducing the risk of pathogens’ contamination on bulb

and stem vegetables and carrots includes scrupulous adherence to hand hygiene by food handlers at all

stages of the supply chain. Employees with symptoms of gastroenteritis should be excluded from

working in food production (i.e. including harvesting and minimal processing) until their symptoms

have subsided.

The equipment should be cleaned and disinfected on a regular basis according to written procedures to

ensure that the potential for cross-contamination is minimized.

All persons involved in handling (cutting, grating, dicing, etc.) of bulb and stem vegetables as well as

carrots for buffets in catering and restaurants should receive hygiene training appropriate to their tasks

and receive periodic assessment while performing their duties to ensure tasks are being completed

with due regard to good hygiene and hygienic practices.

Information should be provided to consumers on appropriate handling of bulb and stem vegetables and

carrots, which should include specific directions for product storage, preparation and intended use.

Consumers should be informed if bulb and stem vegetables as well as carrots are intended to be

consumed as ready-to-eat, and to wash and/or scrub whole or peeled products using potable running


9.3. Specific mitigation options to reduce the risk of Salmonella and Yersinia contamination

As previously considered for leafy greens (EFSA BIOHAZ Panel, 2014c), Salmonella have their

reservoirs in domestic as well as wild animals, birds and humans. The main mitigation options for

reducing the risk of contamination of bulb and stem vegetables as well as carrots are consequently to

prevent direct contact with animal, bird or human faeces as well as indirect contact through slurries,

sewage, sewage sludge, contaminated soil, water, equipment or food contact surfaces or food handlers.

Yersinia enterocolitica and Y. pseudotuberculosis have their reservoirs in the intestinal contents of a

range of animals and are commonly isolated from different environments contaminated by faeces. As

with Salmonella, the main mitigation options for reducing the risk of contamination of bulb and stem

vegetables as well as carrots by Yersinia are consequently to prevent direct contact with animal or

human faeces as well as indirect contact through slurries, sewage, sewage sludge, contaminated soil,

water, equipment or food contact surfaces as well as food handlers. Access of wild animals, such as

birds or rodents should be prevented from premises used for post-harvest processes and storage as is

likely to have occurred in outbreaks in Finland (Kangas et al., 2008).

At primary production, assessment of risks for Salmonella as well as Yersinia contamination from the

environment should aim to reduce risks from previous cultivation or adjacent land use (particularly

when associated with domestic animal production) as well as attractants and harbourage of wild

animals and pests. Particular attention should be paid to appropriate treatment, storage and application

of organic amendments, if used, since these bacteria survive in water, including the possibility of

contaminating water used for irrigation. Care should also be taken to prevent the use of equipment


EFSA Journal 2014;12(12):3937 51

contaminated with Salmonella and Yersinia, particularly segregation from equipment that has come

into contact with animals. Persons handling food during harvesting (as well as during subsequent

minimal processing) are a potential source of Salmonella or Yersinia contamination, and adequate

toilet and hand-washing facilities must be provided at production areas. Scrupulous compliance with

hand hygiene practices such as effective washing is an absolute necessity for all food supply chain

employees, and should be emphasised in local codes of practice and training manuals. Persons with

symptoms of gastroenteritis should be excluded from handling foodstuffs at all stages.

During minimal processing, cooling and washing, all necessary steps to prevent contamination by

Salmonella and Yersinia should be carried out, however these processes, at best, are aimed at

preventing contamination or subsequent growth. Where contamination has occurred at primary

production, even with adequately operated and monitored washing procedures, at best only a 1-2 log

unit reduction is likely to be achieved in the final product. Carrots can be stored at cold temperatures

for several months in high humidity. Decaying carrots are likely to be a substrate for growth of

Y. enterocolitica and Y. pseudotuberculosis. Processors or caterers should not use poor quality carrots.

During distribution, retail, catering and handling in domestic environments, all reasonable steps should

be taken to prevent cross-contamination of Salmonella and Yersinia from other foods, as well as from

food handlers.

As stated previously for leafy greens (EFSA BIOHAZ Panel, 2014c) washing alone will have some

effect in reducing the microbiological (including pathogen) biota whilst also having the potential for

cross-contamination, and identical effects for bulb and stem vegetables and carrots will occur.

Washing with water alone is likely to result in reductions of about 1 log cfu/g of Salmonella and

Yersinia and the use of sanitizers will have an effect on surface contamination by pathogens (as well

as the microbiota); however, this will not guarantee elimination of bacterial foodborne pathogens.

Various sanitizers and other treatments have been evaluated for treating bulb and stem vegetables and

carrots for reducing Salmonella contamination, and these are generally of experimental nature and

provide a low strength of evidence. These treatments included: chlorine and peroxyacetic acid (Ge et

al., 2013); electrolyzed water (Abadias et al., 2008; Park et al., 2008, 2009); ozonated water (Xu and

Wu, 2014); irradiation (Lopez et al., 2005; Dhokane et al., 2006; Song et al., 2006; Murugesan et al.,

2011; Ndoti-Nembe et al., 2013); thermoultrasound and calcium propionate (Kwak et al., 2011); dense

phase carbon dioxide (Liao et al., 2010); essential oils and bacteriocins (Ndoti-Nembe et al., 2013);

high hydrostatic pressure (Nettoo et al., 2011, 2012); carvacrol and cinnamaldehyde (Ravishankar et

al., 2010); and gaseous chlorine dioxide (Sy et al., 2005).

There is no specific information available on the effects of sanitizers and other treatments for reducing

Yersinia in bulb or stem vegetables or carrots.

9.4. Specific mitigation options to reduce the risk of Shigella and Norovirus contamination

Both Norovirus and Shigella have their reservoir in humans. Therefore, the main mitigation options

are good personal hygiene practices by food handlers during harvest, when manually handling produce

during sorting, packing and at the point of final preparation and food service. In addition, mitigation

options include prevention of contamination from other food types as well as food contact surfaces. As

Norovirus as well as Shigella have no proven zoonotic reservoirs, the main sources within the

environment from which contamination of food by Norovirus or Shigella can arise include sewage-

contaminated water and sewage sludge. Hence, at primary production avoiding the use of sewage-

contaminated water and inadequately treated sewage sludge are the main mitigation options for

reducing the risk of Norovirus and Shigella contamination of these vegetables. In contrast to

Norovirus, which may persist for prolonged periods of time in the environment, Shigella cells are,

once excreted from the human host, quite sensitive to environmental conditions and may die rapidly,

especially when exposed to direct sunlight or drying (Binet and Lampel, 2013).


EFSA Journal 2014;12(12):3937 52

As was discussed previously for tomato production (EFSA BIOHAZ Panel, 2014d), information on

existing preventive measures suitable for controlling Norovirus contamination which are in place

according to current EU legislation, and control options for FoNAO can be found in Sections 6.2 of

the scientific opinion of the EFSA BIOHAZ Panel (EFSA Panel on Biological Hazards (BIOHAZ),

2011a), and in the Codex Guidelines on the application of general principles of food hygiene to the

control of virus contamination of food (CAC, 2012). The available guidance is general and does not

refer specifically to individual food commodities such as bulb and stem vegetables or carrots, although

Annex 2 “Control of hepatitis A and Norovirus in fresh produce” of the Codex Guidelines should be

directly applicable to these food categories. The same information may be applicable for the

prevention of Shigella contamination.

Overall it is recommended that only clean or potable water be used during production and minimal

processing, and corrective actions should be taken if contamination occurs. Possible corrective actions

include disinfection e.g. by chlorine. The equipment that comes in contact with food should be

effectively cleaned and, where necessary, disinfected. The efficacy of currently available water and

surface disinfection treatments against Norovirus is not fully certain, and EFSA has recommended

(EFSA Panel on Biological Hazards (BIOHAZ), 2011b) that effort should be focussed on avoiding

viral contamination rather than trying to remove/inactivate viruses in food. Shigella are quite

susceptible to conventional disinfection treatments, therefore prevention of Shigella contamination by

adherence to good hygienic practices in primary production, minimal processing and preparation are

recommended.

Employees with symptoms of gastroenteritis should be excluded from working in food production (i.e.

including harvesting and minimal processing) until their symptoms have subsided, e.g. for 48 hours.

However, as pre- and post-symptomatic shedding can occur, this exclusion may not be entirely

sufficient to prevent the possibility of food contamination from occurring, and returning employees

should pay special attention to hand hygiene. Scrupulous compliance with hand hygiene practices such

as effective washing is an absolute necessity for all food supply chain employees, and should be

emphasised in local codes of practice and training manuals, both in developed and developing

countries.

Wang et al. (2013b) investigated the physical removal of Murine Norovirus, a human Norovirus

surrogate, from contaminated produce items including carrots and celery by scrubbing under running

water with a nylon brush or scouring pad and by peeling. The degree and extent of utensil

contamination with viruses during these operations in the presence and absence of food residue was

also investigated. Scrubbing or peeling resulted in significant levels of virus removal, ranging from

0.93 to 2.85 log PFU. However, utensil cross-contamination occurred and after preparation of a

contaminated produce item, utensil cross-contamination resulted in virus detection on seven

successively prepared produce items. Thus, scrubbing and peeling produce can reduce levels of

viruses on contaminated produce, but the importance of utensil sanitation to prevent cross-

contamination is highlighted.

Green onions inoculated with human NoV surrogates were treated with UV (240 mJ s/cm2), ozone

(6.25 ppm for 10 min), pressure (500 MPa, for 5 min at 20 °C), or sprayed with calcium hypochlorite

(150 ppm, 4 °C). Both Murine Norovirus (MNV) and human adenovirus type 41 (Ad41) were

inoculated either on the surface through spot inoculation or through inoculating contaminated

hydroponic solution allowing for uptake of the virus into the internal tissues. Both surface inoculated

viruses and viruses internalized in green onions were inactivated to some extent by these post-harvest

minimal processing treatments. Viral inactivation for both surrogate viruses was greatest after pressure

treatment, followed by ozone treatment, and the lowest inactivation was observed after chlorine and

UV treatment (Hirneisen and Kniel, 2013b). It has been shown that treatment of green onions

inoculated with MNV with ozone (6.25 ppm) achieved a > 2-log reduction was after 1 min of ozone

treatment (Hirneisen et al., 2011).


EFSA Journal 2014;12(12):3937 53

10. Data on occurrence of E. coli on bulb and stem vegetables and carrots and use of E. coli

as an indicator

There is no routine or regular monitoring of bulb and stem vegetables or carrots for the presence of E.

coli in the EU Member States and there are limited data on the occurrence of E. coli in/on these

vegetables in the peer-reviewed world literature (Table 7). There are limited data available from

studies on the occurrence of E. coli in/on these vegetables, and some of these studies are small (e.g.


making meaningful comparisons between individual studies difficult and in establishing the

representativeness of the data on occurrence of the bacterium. Some of the samples were collected

outside the EU. Consequently there are difficulties in both making meaningful comparisons between

individual studies as well as assessing the representativeness of these data to estimate the overall

levels of contamination.

Since there is a lack of data on the occurrence and levels of E. coli in bulb and stem vegetables as well

as carrots, it is not currently possible to establish relationships between production and minimal

processing practices and numbers of E. coli. However, as previously discussed for leafy greens (EFSA

BIOHAZ Panel, 2014c), E. coli is commonly present in faecal material and has general use as a

hygiene indicator. Consequently, because E. coli is present in high numbers in faecal material (e.g.

fresh manure) and likely to decline in the soil and on the surfaces of bulb and stem vegetables as well

as carrots during primary production, it can be considered as an indicator of a recent exposure to risk

factors for Salmonella as well as for Shigella and Yersinia. However, there is currently insufficient

available data to assess the effectiveness of E. coli criteria to verify compliance to Good Agricultural

Practices (GAP), Good Hygiene Practices (GHP), Good Manufacturing Practices (GMP) and food

safety managements systems (including HACCP) in the production and minimal processing of bulb

and stem vegetables as well as carrots.

11. Microbiological criteria for bulb and stem vegetables and carrots

Considering the limited evidence for both the occurrence and public health risks from contamination

of Salmonella, Shigella, Yersinia and Norovirus in the primary production and minimal processing of

bulb and stem vegetables and carrots, no conclusions can be made on the impact of the establishment

of microbiological Hygiene Criteria, Process Hygiene Criteria or Food Safety Criteria on public

health. However, it is still important that the mitigation options mentioned in Section 9 (including

general hygiene rules and food safety management systems) are applied in order to avoid bulb and

stem vegetables and carrots becoming vehicles of transmission of both zoonotic and non-zoonotic

pathogenic micro-organisms to humans.


EFSA Journal 2014;12(12):3937 54

Table 7: Occurrence of Escherichia coli in bulb and stem vegetables and carrots

Sampling

place Commodity

Sampling


Number

of

samples

analysed

Number

of

positive

samples

% of

positive

samples

95 % CI(a) Detection

limit E. coli levels Reference

Retail

(distribution

centres and

markets)

Scallions and

green onions

Canada Petrifilm 173 11 6.4 [3.4, 10.7] <5 cfu/g <5-7.600 cfu/g (Arthur et al., 2007)

Retail Pre-packed

crudités

UK BS 4285, violet red

bile agar pour plate

247 33 13 [9.6, 18]

<1cfu/g 13% >1cfu/g ;

4% >10 cfu/g ;

2% >102 cfu/g

(Liitle et al., 1997)

Retail

supermarkets

Grated carrot Spain ISO 7251:2005(b)

MPN

18 0 0 [0, 12.9] MPN NA (Abadias et al., 2008)

Retail farmer’s

markets

Carrots Canada Health Canada

MFHPB-19 MPN

206 9 4.4 [2.2, 7.8] MPN Mean 1.21 log

mpn/g

(Bohaychuk et al., 2009)

Retail farmer’s

markets

Green onions Canada Health Canada

MFHPB-19 MPN

129 7 5.4 [2.5, 10.4] MPN Mean 1.43 log

mpn/g

(Bohaychuk et al., 2009)

Retail markets

and street

vendors

Green onion Saudi Arabia Eosin methylene

blue agar (AOAC

Compendium of

Methods for

Microbiological

examination of

Foods 2001)

6 0 0 [0, 33] NA NA (Hassan et al., 2011)

Retail markets

and street

vendors

Celery Saudi Arabia Eosin methylene

blue agar (AOAC

Compendium of

Methods for

Microbiological

examination of

Foods 2001)

8 1 12.5 [1.4, 45.4] NS Mean = 1 log cfu/g (Hassan et al., 2011)

Minimal

processing

plants

Washed

whole, peeled,

cut and grated

carrots

Finland

Violet red bile agar

surface plate

32 0 0 [0, 7.5] <1 cfu/g NA (Maatta et al., 2013)

Restaurants Carrot juice Mexico NS 280 152 54.3 [48.4, 60.1] 3 MPN/ml <3-460 MPN/ml (Torres-Vitela et al., 2013)

Retail markets Celery USA MPN 10 0 0 [0, 21.7] NS NA (Thunberg et al., 2002)


(b): ISO 7251:2005: Microbiology of food and animal feeding stuffs - Horizontal method for the detection and enumeration of presumptive Escherichia coli - Most probable number technique.

International Organization for Standardization, Geneva, Switzerland.


EFSA Journal 2014;12(12):3937 55

CONCLUSIONS AND RECOMMENDATIONS

CONCLUSIONS

Bulb and stem vegetables, for the scope of this scientific opinion, are defined according to

commercial production and consumption and correspond to the botanically true bulbs of

onions (Allium cepa L., Allium fistulosum L.), shallot (Allium cepa L.), the composite bulb of

garlic (Allium sativum L.); the bundle of leaf sheath of the leek (Allium ampeloprasum L.); the

bulb-like fleshy petioles bases of the Florence fennel (Foeniculum vulgare Mill.); the young

shoots of asparagus (Asparagus officinalis L.); the fleshy petiole of celery (Apium graveolens

L.).

Carrots (Daucus carota L.), for the scope of this opinion, are defined according to commercial

production and consumption as a root vegetable commonly orange.

Emphasis is given here to vegetable types associated with public health risks, i.e. carrots,

onion and garlic.


products, and these steps include selection, washing, cleaning, cutting, packaging and storage.

Other types of minimal processing (e.g. commercial unpasteurized juicing etc.) rarely occur

outside retail and catering. Freezing may take place, but this will typically involve a heat

blanching process and is outside the scope of this opinion, although frozen sliced onion may

not be blanched.

Bulb and stem vegetables as well as carrots may be subject to cooking, drying, bottling,

canning and other processes but these are also outside the scope of this opinion.

Despite the variety of types of bulb and stem vegetables as well as carrots produced and

consumed, there is very little or no specific information for interactions with, risk factors,

mitigation options and occurrence of Salmonella, Yersinia, Shigella or Norovirus. Most

information is available for Salmonella and carrots, although this is very limited.

Consequently, in addition to the limited data, conclusions are drawn through what is generally

understood about the properties of these pathogens as well as information from other fresh

produce.

Onion, garlic and carrots grow in the soil and stem vegetables such as celery have prolonged

direct contact with soil during growth and/or harvesting, particularly when celery is blanched.

When consumed as ready-to-eat or minimally processed products, these vegetables are

normally not subjected to physical interventions that will eliminate the occurrence of these

pathogens.

Answers to the Terms of Reference

TOR 3. To identify the main risk factors for the specific food/pathogen combinations identified

under ToR 2, including agricultural production systems, origin and further processing.

The risk factors at primary production for the contamination of bulb and stem vegetables as

well as carrots with Salmonella, Yersinia, Shigella and Norovirus are poorly documented in

the literature, with limited available data but are likely to include the following, based on what

is known for other pathogens or other fresh produce:

o environmental factors, in particular proximity to animal-rearing operation and

climatic conditions that increase the transfer to pathogens from their reservoirs to the

bulb and stem vegetables and carrot growing areas;


EFSA Journal 2014;12(12):3937 56

o animal reservoirs (domestic or wild life) gaining access to growing areas for bulb and

stem vegetables or carrots;

o contamination or cross-contamination by equipment at harvest or post-harvest, and by

manipulation by workers if this takes place at primary production;

o use of untreated or insufficiently treated organic amendments;

o use of contaminated agricultural water either for irrigation or for application of

agricultural chemicals such as pesticides.

Processes at primary production which wet the external portions of the crop close to harvest

represent the highest risk and these include spraying prior to harvest, direct application of

fungicides and other agricultural chemicals and overhead irrigation.

During minimal processing, contamination or cross-contamination via equipment, water or

food handlers are likely to be the main risk factors for contamination with Salmonella,

Yersinia, Shigella and Norovirus of bulb and stem vegetables as well as carrots.

There is limited information on the behaviour of Salmonella, Yersinia, Shigella or Norovirus

in the specific vegetable food matrices but these pathogens are likely to survive on the

surfaces of these vegetables for days to several weeks at both ambient and at refrigeration

temperatures.

At distribution, retail and catering and in domestic and commercial environments,

contamination and cross-contamination, in particular via direct or indirect contact between

raw contaminated food and bulb and stem vegetables is a risk factor for Salmonella, Yersinia,

Shigella and Norovirus. Cross-contamination risks include salad bar environments.

At distribution, retail, catering and in domestic or commercial environments, infected food

handlers are also risk factors (particularly for Norovirus and Shigella). Contamination can be

direct or indirect via poor hand hygiene or food contact surfaces. These contamination and

cross-contamination risks include salad bar environments.

TOR 4. To recommend possible specific mitigation options and to assess their effectiveness and

efficiency to reduce the risk for humans posed by food/pathogen combinations identified under

ToR 2.

Appropriate implementation of food safety management systems including Good Agricultural

Practices (GAP), Good Hygiene Practices (GHP) and Good Manufacturing Practices (GMP)

should be the primary objective of operators producing bulb and stem vegetables as well as

carrots. These food safety management systems should be implemented along the farm to fork

continuum and will be applicable to the control of a range of microbiological hazards.

Salmonella have their reservoirs in domestic as well as wild animals, birds and humans. The

main mitigation options for reducing the risk of contamination of bulb and stem vegetables as

well as carrots are consequently to prevent direct contact with animal, bird or human faeces as

well as indirect contact through slurries, sewage, sewage sludge, contaminated soil, water,

equipment or food contact surfaces or food handlers.

Yersinia enterocolitica and Yersinia pseudotuberculosis have their reservoirs in the intestinal

contents of a range of animals and are commonly isolated from different environments

contaminated by faeces. The main mitigation options for reducing the risk of contamination of

bulb and stem vegetables as well as carrots by Yersinia are consequently to prevent direct

contact with animal or human faeces as well as indirect contact through slurries, sewage,


EFSA Journal 2014;12(12):3937 57

sewage sludge, contaminated soil, water, equipment or food contact surfaces as well as food

handlers.

Both Norovirus and Shigella have their reservoirs in humans. Therefore, the main mitigation

options are good personal hygiene practices by food handlers during harvest, manual handling

during sorting, packing and at the point of final preparation and food service. In addition,

mitigation options include prevention of cross-contamination from other food types as well as

food contact surfaces.

The main sources within the environment from which contamination of food by Norovirus or

Shigella can arise include sewage-contaminated water and sewage sludge. Hence, at primary

production avoiding the use of sewage-contaminated water and inadequately treated sewage

sludge, are the main mitigation options for reducing the risk of Norovirus and Shigella

contamination of these vegetables.

Production areas should be evaluated for hazards that may compromise hygiene and food

safety, particularly to identify potential sources of faecal contamination. If the evaluation

concludes that contamination in a specific area is at levels that may compromise the safety of

crops, in the event of heavy rainfall and flooding for example, intervention strategies should

be applied to restrict growers from using this land for production of these vegetables until the

hazards have been addressed.

Each farm environment (including open field or greenhouse production) should be evaluated

independently as it represents a unique combination of numerous characteristics that can

influence occurrence and persistence of pathogens in or near bulb and stem vegetables as well

as carrot growing areas.

Attention should be paid to the selection of the water sources for irrigation, agricultural

chemical application (e.g. fungicide) and in particular to the avoidance of the use or the

ingress of water contaminated by sewage.

Both water treatment or efficient drainage systems that take up excess overflows are possible

mitigation options to prevent the additional dissemination of contaminated water.

Risks posed by water should be minimised by assessing the microbial quality of the sources of

water used on the farm for the presence of pathogens. Since Escherichia coli is an indicator

micro-organism for faecal contamination in irrigation water, growers should arrange for

periodic testing to be carried out to inform preventive measures.

Appropriate production, treatment, storage, management and use of manure or sludge is

important.

During minimal processing, GMP and food safety management systems (including HACCP)

will assist Salmonella, Yersinia, Shigella and Norovirus risk mitigation strategies.

It is recommended that water used during minimal processing be monitored to assess its

microbial quality.

When disinfectants are used in wash water the concentration should be monitored to verify

that they are applied effectively to reduce the potential risk of cross-contamination while

avoiding the accumulation of disinfection by-products.

The main mitigation options for reducing the risk of pathogen contamination of bulb and stem

vegetables and carrots during minimal processing includes scrupulous adherence to hand


EFSA Journal 2014;12(12):3937 58

hygiene by food handlers at all stages of the supply chain. Employees with symptoms of

gastroenteritis should be excluded from working in food production (i.e. including harvesting

and minimal processing) until their symptoms have subsided.

Equipment should be cleaned and disinfected on a regular basis according to written

procedures to ensure that the potential for cross-contamination is minimized.

All persons involved in handling (cutting, grating, dicing, etc.) of bulb and stem vegetables as

well as carrots for buffets in catering and restaurants should receive hygiene training

appropriate to their tasks and receive periodic assessment while performing their duties to

ensure tasks are being completed with due regard to good hygiene and hygienic practices.

Information should be provided to consumers on appropriate handling of bulb and stem

vegetables and carrots, which should include specific directions for product storage,

preparation and intended use.

Consumers should be informed if bulb and stem vegetables as well as carrots are intended to

be consumed as ready-to-eat, and, to scrub whole or peeled products using potable running


TOR 5. To recommend, if considered relevant, microbiological criteria for the identified specific

food/pathogen combinations throughout the production chain.

There is no routine or regular monitoring of bulb and stem vegetables or carrots for the

presence of Salmonella, Yersinia, Shigella and Norovirus in the EU Member States and there

are limited data on the occurrence of these pathogens in/on these vegetables in Europe.

There are limited studies available in the peer-reviewed world literature on the occurrence of

Salmonella, Yersinia, Shigella and Norovirus on/in bulb and stem vegetables or carrots. There

are difficulties in making meaningful comparisons between individual studies as well as

assessing the representativeness of these data to estimate the overall levels of contamination.

Considering the limited evidence for both the occurrence and public health risks from

contamination of Salmonella, Shigella, Yersinia and Norovirus in the primary production and

minimal processing of bulb and stem vegetables and carrots, no conclusions can be made on

the impact of the establishment of microbiological Hygiene Criteria, Process Hygiene Criteria

or Food Safety Criteria on public health.

There is a lack of data on the occurrence and levels of E. coli in bulb and stem vegetables as

well as carrots. Thus, the effectiveness of E. coli criteria to verify compliance to Good

Agricultural Practices (GAP), Good Hygiene Practices (GHP), Good Manufacturing Practices

(GMP) and food safety management systems (including HACCP) in the production and

minimal processing of bulb and stem vegetables as well as carrots cannot be assessed.

RECOMMENDATIONS

More detailed categorization of food of non-animal origin should be introduced to allow

disaggregation of the currently reported data collected via EFSA’s zoonoses database on

occurrence and enumeration of foodborne pathogens.

If additional biological hazards or further public health risks are identified with the

consumption of these categories of food of non-animal origin, risk assessment studies may be

needed to inform the level of hazard control that should be achieved at different stages of the

food chain. These studies should be supported by targeted surveys on the occurrence of

foodborne pathogens in such vegetables at specific steps in the food chain to indicate the level


EFSA Journal 2014;12(12):3937 59

of hazard control and efficacy of application of food safety management systems, including

GAP, GHP, GMP and HACCP, that can be achieved.

Further data should be collected to evaluate the suitability of microbiological (e.g. E. coli)

indicators for relevant microbiological hazards in bulb and stem vegetables and carrots during

their production and minimal processing.

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EFSA Journal 2014;12(12):3937 69

APPENDICES

Appendix A. List of questions to be addressed by the European Fresh Produce Association

(Freshfel) and information received from Freshfel on 22 July 2013 and 19 August 2014

1. How do you categorise ‘bulb and stem vegetables’ and carrots according to different:

- production systems,

- processing (excluding thermal treatment or any equivalent (e.g. blanching as well as shelf

stable juices) and

- presentation at retail?

All questions below aim at characterizing the ‘bulb and stem vegetables’ and carrots sector in the EU.

PRODUCTION SECTOR

2. Provide an overview of this sector listing the most commonly produced botanical varieties of

‘bulb and stem vegetables’ in the EU?

3. Which are the top 10 types of ‘bulb and stem vegetables’ produced in EU including carrots?

4. Which are the top 10 types of ‘bulb and stem vegetables’ sold in EU including carrots?

5. Which countries are the major producers in the EU?

6. Which are the main third countries providing the EU with ‘bulb and stem vegetables’ and

carrots?

7. Which is the share of the market covered by imported production versus intra-EU production

of ‘bulb and stem vegetables’ and carrots?

8. What is the share of producers of ‘bulb and stem vegetables’ and carrots which are not

members of Freshfel in the EU?

Which volume of production do these producers represent?

9. Are there any figures in the EU to characterize the proportion of the production of ‘bulb and

stem vegetables’ and carrots from “home/small scale” producers when compared to “large-

scale” production?

10. Provide available figures on (i) production, (ii) producers, (iii) trade, (iv) certification and (v)

distribution (type of outlets) of the ‘bulb and stem vegetables’ and carrots.

11. Indicate, if available the proportion of carrots sold peeled, pre-cut, shredded or whole?

AGRICULTURAL PRODUCTION SYSTEMS

12. Are there any producer’s survey results which could help to describe how ‘bulb and stem

vegetables’ and carrots are produced in the EU?

13. Characterise the profile of workers in the production of ‘bulb and stem vegetables’ and carrots

(e.g. training, casual workers, foreign workers etc).

14. Please indicate percentages of production of ‘bulb and stem vegetables’ and carrots (i) in

fields, (ii) in greenhouses (iii) soilless (hydroponics) or (iv) in soil?

15. Are there any additional production systems in place in the EU (as well as for imported

products)?

16. Which ‘bulb and stem vegetables’ and carrots can be produced as hydroponic crop?

17. Indicate the major irrigation systems and water sources in the agricultural production of ‘bulb

and stem vegetables’ and carrots.

Is the water quality controlled (microbiologically)? If so and if available, provide data on

microbiological quality of the water used in the agricultural production of ‘bulb and stem

vegetables’ and carrots.


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PROCESSING OF BULB AND STEM VEGETABLES AND CARROTS

18. Which are the most common processing practices for ‘bulb and stem vegetables’ and carrots

in the EU?

19. Which agricultural practices and processing steps - can be executed (i) only manually, (ii) both

manually or mechanically or (iii) preferentially mechanically?

What are the percentages of manual versus mechanical practices?

20. Indicate the major water sources in the processing of ‘bulb and stem vegetables’ and carrots.

Is the water quality controlled (microbiologically)? If so and if available, provide data on

microbiological quality of the water used in the processing of ‘bulb and stem vegetables’ and

carrots.

21. How important is the share of production in the EU for different ‘bulb and stem vegetables’

categories proposed in the scope of the answer to question 1?

Which proportion of ‘bulb and stem vegetables’ and carrots are (i) sold directly (without

further processing) or (ii) undergoing processing (peeling, pre-cutting, shredding, mixing,

packaging and drying)?

DISTRIBUTION AND RETAIL

22. Which are the procedures and conditions for transport and distribution of ‘bulb and stem

vegetables’ and carrots in the EU?

Are there any specific cooling practices in place for bulb and stem vegetables (e.g. asparagus)

at harvest or post-harvest storage (or long distance transport)?

23. Are there any specific control measures in place in the EU to maintain the cold chain during

storage and distribution of ‘bulb and stem vegetables’ and carrots?

Are there any specific control measures in place to maintain long term storage?

24. Which proportion of ‘bulb and stem vegetables’ and carrots may be sold without temperature

control during distribution in the EU?

25. Describe how traceability of ‘bulb and stem vegetables’ and carrots is addressed for the

different agricultural production systems and processing options?

SYSTEMS IN PLACE TO ENSURE SAFETY OF PRODUCTS

26. Are there any European guidelines/codes available from Freshfel or other associations of

producers on practices (including peeling, pre-cutting, shredding, mixing, packaging and

drying) to ensure food safety in the production of ‘bulb and stem vegetables’ and carrots?

27. In your view, what are the strengths and weaknesses of the current GAPs, GMPs and

standards to ensure microbiological quality of ‘bulb and stem vegetables’ and carrots?

28. In your view, which are the major weak points from the microbiological point of view in the

agricultural production systems as well as in the processing of ‘bulb and stem vegetables’ and

carrots?

29. Do the producers of peeled/pre-cut/shredded/mixed/pre-packaged/dry ‘bulb and stem

vegetables’ and carrots in the EU need to be registered as food processing establishments?

30. What are the hygienic requisites that these processing establishments need to comply with?

How is compliance with these hygienic requisites verified?

31. Are there any central repositories of data on non-compliance with the GAPs, GMPs, standards

as well as on the analysis of these data?


EFSA Journal 2014;12(12):3937 71

32. Are there many companies producing ‘bulb and stem vegetables’ and carrots which are

applying the “test to release” for microbiological parameters? If so, are companies using

presence/absence tests? In case enumeration testing is used, which are the threshold levels

(cfu/g) used for interpretation of the analysis results?

33. Are the producers, producer associations or any other stakeholders (e.g. retail) also doing

regular testing/monitoring of ‘bulb and stem vegetables’ and carrots?

34. Which are the sampling plans used in the scope of this testing/monitoring of ‘bulb and stem

vegetables’ and carrots?

35. Is there any additional testing/monitoring in place for imported ‘bulb and stem vegetables’ and

carrots?

36. Does Freshfel have any available data in the EU on levels of detection and enumeration of

Salmonella, Yersinia, Shigella and Norovirus in ‘bulb and stem vegetables’ and carrots?

37. Which methods for detection and enumeration of Salmonella, Yersinia, Shigella and

Norovirus in ‘bulb and stem vegetables’ and carrots are being used in the food chain in the

EU?

38. Which are the differences on the hygienic requisites for the production of organic ‘bulb and

stem vegetables’ and carrots when compared to conventional production?


39. What are the hygienic requisites in place for imported ‘bulb and stem vegetables’ and carrots?


40. Which chemical and/or physical decontamination methods are being used in the EU for the

treatment of soil, substrates, manure or compost?

41. Which chemical and/or physical decontamination methods are being used in the EU for the

treatment of water (reservoirs, irrigation systems, processing water)?

42. Describe the practices in use in the EU for chemical and/or physical decontamination of ‘bulb

and stem vegetables’ and carrots? Which are the main methods in place in the EU?

43. Which chemical and/or physical decontamination methods are allowed in the EU among

Member States?

44. Does Freshfel provide specific recommendations on methods used to reduce contamination of

‘bulb and stem vegetables’ and carrots by Salmonella, Yersinia, Shigella and Norovirus?


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Appendix B. Bulb and stem vegetables and carrots production statistics tables (EUROSTAT,

FAOSTAT) (provided by Freshfel on 19 August 2014

Table 8: Onion production in metric tons (Source: FAOSTAT)

Producing Country 2007 2008 2009 2010 2011 Share in

2011

Netherlands 1 117 000 1 269 362 1 303 755 1 337 060 1 577 877 21.9 %

Spain 1 218 528 1 100 540 1 304 120 1 151 900 1 394 804 19.3 %

Poland 752 468 618 233 707 792 577 983 676 956 9.4 %

Germany 428 058 464 405 505 640 447 077 581 324 8.1 %

France 229 830 194 594 227 724 387 908 499 500 6.9 %

Italy 371 452 403 521 384 418 380 855 413 793 5.7 %

Romania 324 993 395 579 378 106 369 142 394 305 5.5 %

Extra EU 443 779 383 758 272 692 309 424 333 717 4.6 %

United Kingdom 323 950 364 550 368 800 378 900 315 700 4.4 %

Greece 188 630 224 400 218 607 212 292 267 649 3.7 %

Austria 97 620 122 608 139 428 154 104 200 497 2.8 %

Portugal 120 500 126 100 127 300 132 915 117 721 1.6 %

Belgium 66 200 72 700 78 300 82 319 76 376 1.1 %

Denmark 55 000 55 800 54 628 52 270 62 940 0.9 %

Hungary 70 333 69 789 63 154 42 676 59 118 0.8 %

Czech Republic 40 424 41 505 38 765 34 653 45 631 0.6 %

Sweden 28 000 30 000 33 084 31 500 41 623 0.6 %

Slovakia 22 662 28 544 26 394 28 222 35 743 0.5 %

Finland 22 918 20 602 21 883 19 991 24 754 0.3 %

Lithuania 17 578 29 582 20 574 19 034 24 189 0.3 %

Bulgaria 16 813 22 395 14 473 25 446 22 437 0.3 %

Latvia 16 687 17 270 29 799 16 292 20 200 0.3 %

Ireland 8 700 10 056 10 295 10 094 9 244 0.1 %

Malta 6 537 6 475 7 645 8 478 7 981 0.1 %

Slovenia 4 520 5 343 5 997 4 667 6 333 0.1 %

Estonia 1 353 2 440 1 914 2 155 1 301 0.0 %

Luxembourg 92 66 81 40 75 0.0 %

Cyprus 78 75 70 70 71 0.0 %

Total 5 994 703 6 080 292 6 345 438 6 217 467 7 211 859 100.0 %


EFSA Journal 2014;12(12):3937 81

Table 9: Onion import from intra-EU in metric tons (Source: EUROSTAT)

Importing country 2007 2008 2009 2010 2011 2012 Share in

2012

United Kingdom 265 134 272 186 280 563 281 692 278 345 252 788 21.1 %

Germany 210 492 218 031 198 699 240 287 222 079 178 145 14.8 %

Belgium 110 695 121 596 114 941 110 518 116 526 118 232 9.9 %

France 105 163 109 996 93 303 86 928 84 408 99 606 8.3 %

Netherlands 72 198 65 552 118 950 88 273 92 935 82 445 6.9 %

Italy 51 684 56 444 62 378 58 321 52 387 56 981 4.7 %

Poland 69 868 78 531 50 629 106 840 84 472 55 974 4.7 %

Czech Republic 59 452 56 591 59 489 60 399 56 689 52 545 4.4 %

Portugal 43 707 36 244 35 880 36 674 37 671 45 286 3.8 %

Spain 26 358 52 746 58 880 41 881 36 116 34 984 2.9 %

Romania 11 226 17 834 19 114 17 370 24 760 33 223 2.8 %

Sweden 30 731 22 212 24 727 29 606 31 367 32 091 2.7 %

Ireland 34 952 45 405 31 724 32 989 31 388 28 886 2.4 %

Slovakia 17 287 19 474 16 527 18 239 23 655 17 407 1.5 %

Austria 19 835 23 147 22 832 25 018 19 442 14 734 1.2 %

Lithuania 11 020 15 324 11 176 14 420 16 127 13 840 1.2 %

Slovenia 10 810 13 261 13 458 12 723 12 438 12 476 1.0 %

Bulgaria 1 283 774 4 915 7 245 10 108 12 039 1.0 %

Denmark 10 547 11 281 11 877 14 182 13 129 11 381 0.9 %

Finland 6 041 5 773 7 373 6 061 9 217 11 346 0.9 %

Hungary 14 631 13 573 17 829 14 621 12 145 10 258 0.9 %

Latvia 4 055 6 289 6 416 8 375 6 895 8 234 0.7 %

Estonia 3 824 4 600 6 560 6 893 6 141 5 830 0.5 %

Cyprus 675 1 797 2 438 2 982 3 578 4 093 0.3 %

Greece 4 186 6 711 7 715 6 447 5 672 3 191 0.3 %

Luxembourg 1 553 1 593 1 450 3 640 3 374 3 102 0.3 %

Malta 512 895 734 338 590 754 0.1 %

Total 1 197 919 1 277 860 1 280 577 1 332 962 1 291 654 1 199 871 100.0 %


EFSA Journal 2014;12(12):3937 82

Table 10: Onion import from extra-EU in metric tons (Source: EUROSTAT)

Exporting Country 2007 2008 2009 2010 2011 2012 Share in

2012

New Zealand 109 914 115 476 88 073 90 921 70 803 77 259 31.5 %

Egypt 63 943 47 104 36 325 62 961 73 644 53 197 21.7 %

Australia 35 917 37 441 33 806 32 973 39 899 38 915 15.9 %

Chile 35 259 43 500 24 153 47 563 57 514 20 775 8.5 %

Mexico 8 220 10 951 14 000 8 808 12 747 11 669 4.8 %

India 9 318 16 298 11 056 13 994 11 805 10 945 4.5 %

Peru 2 254 3 219 2 320 3 689 5 090 6 919 2.8 %

Macedonia 5 814 2 223 1 070 1 453 3 600 6 157 2.5 %

Argentina 52 710 28 203 29 839 10 731 22 313 4 441 1.8 %

Turkey 58 438 46 057 10 089 14 695 13 924 3 103 1.3 %

Others 61 992 33 286 21 961 21 636 22 378 12 090 4.9 %

Total 443 779 383 758 272 692 309 424 333 717 245 470 100.0 %

Table 11: Garlic production in metric tons (Source: FAOSTAT)

Producing Country 2007 2008 2009 2010 2011 Share in

2011

Spain 151 674 133 610 154 000 136 561 139 882 38.3 %

Extra-EU 93 082 84 015 77 625 73 188 81 997 22.5 %

Romania 49 948 72 333 63 245 67 215 66 602 18.2 %

Italy 28 800 26 958 26 403 29 655 30 585 8.4 %

France 20 447 19 673 20 148 17 933 19 403 5.3 %

Greece 10 459 10 700 10 000 9 500 10 500 2.9 %

Hungary 5 156 4 685 4 399 4 171 6 466 1.8 %

Slovakia 2 772 2 129 2 121 2 141 2 223 0.6 %

Lithuania 2 728 2 862 2 916 1 790 1 796 0.5 %

Portugal 1 800 1 860 1 900 1 984 1 757 0.5 %

Bulgaria 1 197 1 153 1 555 2 263 1 665 0.5 %

Malta 438 552 659 516 537 0.1 %

Austria 222 276 263 308 483 0.1 %

Slovenia 254 301 307 292 449 0.1 %

Czech Republic 2 038 1 759 210 222 322 0.1 %

Estonia 178 165 74 110 167 0.0 %

Latvia 828 145 66 118 144 0.0 %

Cyprus 191 163 154 155 141 0.0 %

Finland 22 16 12 17 32 0.0 %

Total 372 234 363 355 366 057 348 139 365 151 100.0 %


EFSA Journal 2014;12(12):3937 83

Table 12: Garlic import from intra-EU in metric tons (Source: EUROSTAT)


2012

Italy 17 287 16 677 19 569 20 758 23 989 22 684 19.5 %

Germany 16 155 15 257 16 659 17 322 16 818 17 575 15.1 %

France 15 321 12 028 11 958 14 489 14 133 14 587 12.6 %

Portugal 7 599 7 332 7 389 7 616 7 138 11 182 9.6 %

United Kingdom 14 381 12 385 10 934 11 138 17 268 9 724 8.4 %

Czech Republic 5 515 4 812 5 025 4 836 5 223 6 980 6.0 %

Belgium 2 632 2 730 2 906 3 376 3 649 4 699 4.0 %

Austria 3 573 4 243 4 120 4 107 3 918 3 839 3.3 %

Netherlands 4 165 3 488 4 398 3 392 4 136 3 699 3.2 %

Spain 3 253 3 865 2 867 2 566 3 583 3 397 2.9 %

Poland 3 009 3 115 3 282 3 067 2 164 2 793 2.4 %

Sweden 2 557 2 437 2 419 2 486 3 258 2 669 2.3 %

Slovakia 2 404 2 658 2 183 1 636 1 737 2 018 1.7 %

Romania 452 549 554 573 1 309 1 405 1.2 %

Lithuania 825 908 1 227 1 574 1 551 1 334 1.1 %

Ireland 1 357 2 174 1 120 1 144 1 114 1 333 1.1 %

Hungary 176 399 559 814 589 1 054 0.9 %

Slovenia 652 937 1 260 963 699 821 0.7 %

Greece 1 285 1 141 1 096 1 030 1 234 791 0.7 %

Finland 895 994 958 868 808 790 0.7 %

Latvia 631 620 677 631 659 737 0.6 %

Denmark 1 274 1 240 1 092 651 724 658 0.6 %

Bulgaria 315 378 421 509 681 508 0.4 %

Estonia 373 296 377 346 315 302 0.3 %

Luxembourg 340 312 278 291 269 266 0.2 %

Cyprus 100 84 125 141 219 140 0.1 %

Malta 176 235 193 105 195 92 0.1 %

Total 106 702 101 294 103 646 106 429 117 380 116 077 100.0 %


EFSA Journal 2014;12(12):3937 84

Table 13: Garlic import from extra-EU in metric tons (Source: EUROSTAT)

Exporting Country 2007 2008 2009 2010 2011 2012 Share in

2012

China 63 853 56 795 51 569 48 270 53 145 42 982 60.6 %

Argentina 18 209 19 331 19 035 17 450 17 344 16 330 23.0 %

Egypt 3 551 2 637 2 388 2 348 4 217 4 790 6.8 %

Chile 1 714 1 272 1 755 1 711 3 066 3 217 4.5 %

Mexico 1 962 2 219 2 009 2 424 2 881 3 153 4.4 %

USA 535 210 153 239 377 174 0.2 %

Brazil 1 032 447 88 - 149 72 0.1 %

Turkey 86 79 73 470 185 51 0.1 %

Zimbabwe 26 10 7 9 12 29 0.0 %

India 572 1 5 - 3 29 0.0 %

Tunisia 2 16 29 7 1 23 0.0 %

Morocco 409 250 60 117 412 23 0.0 %

Peru 24 123 42 44 - 22 0.0 %

Madagascar 10 16 16 24 13 11 0.0 %

Other 1 096 611 395 74 192 19 0.0 %

Total 93 081 84 017 77 624 73 187 81 997 70 925 100.0 %


EFSA Journal 2014;12(12):3937 85

Table 14: Carrot production in metric tons (Source: FAOSTAT)

Producing Country 2007 2008 2009 2010 2011 2012 Share in

2012

Poland 938 230 817 024 913 304 764 585 887 374 834 698 15.2 %

United Kingdom 752 277 719 270 718 700 763 100 694 104 663 700 12.1 %

Germany 562 296 547 073 570 239 553 972 533 717 592 761 10.8 %

France 312 612 301 495 636 469 601 904 624 459 544 979 9.9 %

Netherlands 543 000 496 000 561 000 481 000 482 000 511 000 9.3 %

Italy 565 300 594 800 523 330 489 171 542 691 482 302 8.8 %

Spain 426 074 414 517 420 000 424 300 268 100 377 400 6.9 %

Belgium 269 800 288 900 326 100 314 100 317 400 317 400 5.8 %

Romania 185 094 234 752 215 346 221 082 245 508 200 475 3.6 %

Portugal 150 000 154 000 156 000 162 881 144 262 150 000 2.7 %

Sweden 89 400 91 600 122 600 83 000 104 870 128 700 2.3 %

Austria 74 246 80 849 83 587 85 631 109 044 98 272 1.8 %

Extra-EU 53 945 58 657 108 744 85 475 76 622 93 371 1.7 %

Denmark 70 000 67 299 91 590 104 830 107 240 84 858 1.5 %

Hungary 119 200 75 151 65 628 58 532 65 149 74 721 1.4 %

Lithuania 62 712 56 973 63 716 40 895 70 478 67 800 1.2 %

Finland 68 351 60 751 70 608 67 509 72 758 55 751 1.0 %

Greece 43 619 47 600 45 000 43 600 54 800 53 300 1.0 %

Slovakia 31 817 37 155 35 654 34 879 42 005 42 005 0.8 %

Latvia 30 408 36 446 43 317 34 307 38 632 28 082 0.5 %

Ireland 25 582 24 595 26 021 25 588 25 503 27 000 0.5 %

Czech Republic 39 466 34 406 22 333 18 834 24 390 20 763 0.4 %

Estonia 20 126 15 556 20 885 22 817 24 517 17 083 0.3 %

Croatia 11 553 7 629 10 954 12 999 10 767 15 294 0.3 %

Bulgaria 10 286 13 437 14 614 10 576 11 997 9 590 0.2 %

Cyprus 1 879 1 899 2 145 1 988 3 254 3 364 0.1 %

Slovenia 2 530 3 280 3 897 2 039 2 974 2 709 0.0 %

Malta 1 450 1 129 1 060 1 365 1 327 981 0.0 %

Luxembourg 203 310 409 478 231 230 0.0 %

Total 5 461 456 5 282 553 5 873 250 5 511 437 5 586 173 5 498 589 100.0 %


EFSA Journal 2014;12(12):3937 86

Table 15: Carrot import from intra-EU in metric tons (Source: EUROSTAT)


2012

Belgium 269 469 301 779 275 932 256 494 276 268 278 629 29.4 %

Germany 198 599 242 126 189 145 231 569 210 168 217 684 23.0 %

France 112 786 112 091 121 525 116 270 113 131 131 353 13.9 %

Netherlands 34 273 33 564 39 302 30 154 30 392 36 424 3.8 %

Czech Republic 37 314 34 899 37 547 40 135 37 947 36 104 3.8 %

United Kingdom 49 347 46 800 45 883 29 537 32 465 31 339 3.3 %

Portugal 39 801 26 289 22 793 32 910 29 028 28 890 3.0 %

Poland 29 422 42 499 36 457 37 680 40 965 27 366 2.9 %

Ireland 15 935 16 179 19 296 17 150 18 597 19 472 2.1 %

Slovakia 17 765 18 653 15 526 16 977 20 587 18 515 2.0 %

Austria 13 929 20 639 15 483 22 679 20 634 16 297 1.7 %

Romania 7 645 12 368 7 553 9 063 11 197 14 003 1.5 %

Spain 30 807 17 934 13 360 23 341 16 380 13 953 1.5 %

Sweden 13 059 13 784 8 120 7 537 6 597 13 576 1.4 %

Denmark 9 144 10 080 12 276 10 205 8 110 11 343 1.2 %

Lithuania 8 006 15 214 9 613 13 019 11 478 8 296 0.9 %

Hungary 13 594 12 153 11 123 12 445 9 911 7 161 0.8 %

Slovenia 5 123 6 522 5 970 6 182 6 675 6 508 0.7 %

Italy 4 742 7 701 8 401 4 927 5 096 6 011 0.6 %

Latvia 2 988 4 182 5 559 4 094 4 099 5 583 0.6 %

Finland 5 923 6 972 8 114 5 159 4 791 5 449 0.6 %

Luxembourg 2 787 2 553 1 515 4 045 4 136 3 904 0.4 %

Bulgaria 886 512 2 074 3 056 2 198 3 089 0.3 %

Greece 3 639 3 500 3 522 3 464 4 144 2 949 0.3 %

Cyprus 278 289 467 1 586 1 742 1 479 0.2 %

Estonia 1 510 1 500 2 607 1 675 1 316 1 378 0.1 %

Malta 655 1 124 1 284 555 685 527 0.1 %

Total 929 426 1 011 906 920 447 941 908 928 737 947 282 100.0 %


EFSA Journal 2014;12(12):3937 87

Table 16: Carrot import from extra-EU in metric tons (Source: EUROSTAT)

Exporting country 2007 2008 2009 2010 2011 2012 2013 Share in

2013

Israel 11 867 18 086 59 310 42 222 35 457 64 080 66 737 73.4 %

Turkey 34 248 31 970 36 088 33 857 32 114 20 856 14 660 16.1 %

USA 1 386 2 174 2 721 2 907 3 094 2 942 3 395 3.7 %

China 682 625 2 845 2 496 2 530 2 605 2 484 2.7 %

Costa Rica 794 794 395 592 610 1 046 1 491 1.6 %

Mexico - - 92 - - 169 594 0.7 %

South Africa 588 957 300 259 513 636 560 0.6 %

Australia 2 982 2 183 2 608 2 136 961 562 392 0.4 %

Other 784 1 504 3 551 264 680 173 324 0.4 %

Serbia 28 51 164 105 366 214 178 0.2 %

Morocco 586 313 671 637 297 90 81 0.1 %

Total 53 945 58 657 108 745 85 475 76 622 93 373 90 896 100.0 %


EFSA Journal 2014;12(12):3937 88

GLOSSARY

Bulbs are storage organs for biennial plants and thus they must survive a winter period. They are

formed by modified, fleshy leaves rich in nutrients (scales), surrounding a bud from which the plant

will grow after the winter period. They have evolved various protective measures including the

formation of dry external tunics, the biosynthesis of natural products, which act as feeding deterrents

for insects and small mammals as well as antimicrobial agents. The Alliums including onions, shallots,

garlic and leeks fall into this class (Hanson, 2011).The Onion and shallot bulb contain one single bud,

whereas the garlic bulb is a complex bulb consisting of several small bulbs (also called garlic cloves),

each containing one bud.

Carrots (Daucus carota L.) are biannuals root vegetables of the Apiaceae family. The edible portion

is the storage taproot, which contains high levels of carbohydrates (sugars) and ß-carotene (pre-

vitamin A). In general, high quality carrots are firm, straight from “shoulder” to “tip,” smooth with

little residual “hairiness,” sweet with no bitter or harsh taste, and show no signs of cracking or

sprouting (Suslow et al., 2002).

Celery (Apium graveolens L.) is a biennial stem vegetable from the Apiaceae family but is planted

and harvested as an annual crop. The edible portion is the long, thick, green fleshy petioles and, if

present after trimming, associated leaves. High quality celery consists of stalks which are well formed,

have thick petioles, are compact (not significantly bowed or bulging), have minimal petiole twisting,

and have a light green and fresh appearance (Suslow and Cantwell, 1998).

Clean water is clean seawater (natural, artificial or purified seawater or brackish water that does not

contain micro-organisms, harmful substances or toxic marine plankton in quantities capable of directly

or indirectly affecting the health quality of food) and fresh water of a similar quality (Regulation (EC)

No 852/2004).27

Decontamination treatments are mechanical, physical, and chemical treatments, which are applied to

eliminate contaminants, including microbial contamination. They can be applied to water, surfaces,

equipment and areas.

Disinfectants are agents or systems that kill or eliminate bacteria found on inanimate surfaces or

environments. Within this opinion, disinfectant agents or systems are defined as those

decontamination agents applied to eliminate micro-organisms in wash water.

Garlic (Allium sativum L.), is a member of the onion family (Amaryllidaceae). It is a bulb comprised

of cloves (thickened storage leaves) individually wrapped in dried leaf sheaths or skins attached to a

compressed stem plate. The whole bulb is also wrapped in several layers of dried leaf sheaths. Garlic

is produced as an annual crop for seed, fresh market, and processed products. High quality garlic bulbs

are clean, white (or other colour typical of the cultivar), and well cured (dried neck and outer skins).

The cloves should be firm to the touch. Cloves from mature bulbs should have a high dry weight and

soluble solids content (SSC) – more than 35 % in both cases (Cantwell, 2014).

Green onions/spring onions, also called spring onions or scallions, are onions (Allium cepa L.),

which are eaten for their immature bulb and green foliage (Adamicki, 2014). Green onions lack a fully

developed root bulb and have a relatively mild onion flavour. For more information see “Onions”.

Fertigation is the application of fertilizers, soil amendments, or other water-soluble products through

an irrigation system.

27 Regulation (EC) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of

foodstuffs. OJ L 139, 30.4.2004, p.1-54.

http://www.theplantlist.org/1.1/browse/A/Amaryllidaceae/


EFSA Journal 2014;12(12):3937 89

Food of non-animal origin include those derived from plants and comprise a wide range of fruit,

vegetables, salads, juices, seeds, nuts, cereals, herbs, spices, fungi and algae, which are commonly

consumed in a variety of forms. Categorisation of FoNAO, as considered in the scope of this scientific

opinion, is discussed in Section 2.2 of EFSA Panel on Biological Hazards (BIOHAZ) (2013b).

Food Safety Criteria are defined in EU legislation for the microbiological acceptability of food

products and are criteria defining the acceptability of a product or a batch of foodstuff applicable to

products placed on the market (Regulation (EC) No 2073/2005).28

If a Food Safety Criterion is not met

for a product or batch of foodstuff, then this should not be placed on the market or, if it already has, be

considered for recall.

Fresh Produce refers to fresh fruits and vegetables that are likely to be sold to consumers in an

unprocessed or minimally processed (i.e. raw) form and are generally considered as perishable. Fresh

produce may be intact, such as strawberries, whole carrots, radishes, and fresh market tomatoes, or cut

during harvesting, such as celery, broccoli, and cauliflower.29

In the scope of this opinion fresh

produce also applies to fresh-cut produce, such as pre-cut, packaged, ready-to-eat salad mixes.

Fungicide is a specific type of pesticide that controls fungal diseases by specifically inhibiting or

killing the fungus or fungal spores.

Good Agricultural Practices (GAP) apply available knowledge to address environmental, economic

and social sustainability for on-farm production and post-production processes resulting in safe and

healthy food and non-food agricultural products (FAO, 2003).

Good Hygiene Practices (GHP) relate to general, basic conditions for hygienic production of a

foodstuff, including requirements for hygienic design, construction and operation of the plant,

hygienic construction and use of equipment, scheduled maintenance and cleaning, and personnel

training and hygiene. A developed and implemented GHP programme is a pre-requisite for HACCP

system (EFSA, 2005).

Good Manufacturing Practices (GMP) cover the principles needed to design plant layout,

equipment and procedures for the production of safe food. This includes hygienic operation and

cleaning and disinfection procedures. The codes and requirements may be formally specified by e.g.

Codex Alimentarius Committee on Food Hygiene (EFSA, 2005).

Harvest is the process of collecting mature crops from the fields and immediate handling.

Hydro-cooling is one of several post-harvest cooling methods available to growers, packers, and

shippers to reduce the temperature of the crops. This technique consist in dumping produce into cold

water, or running cold water over produce to remove heat.

Hydro-coolers produce chilled water and then move this water into contact with the produce.

Hygiene Criteria are criteria indicating the acceptable functioning at pre-harvest, harvest and on farm

post-harvest production prior to processing and are proposed to verify and validate Good Agricultural

Practices (GAP) and Good Hygiene Practices (GHP).

Minimal processing is any action applied to the initial product (e.g. cleaning, coring, peeling,

chopping, slicing or dicing and washing) and which is not included below in the definition of

processing (e.g. heating, smoking, curing, maturing, drying, marinating, extraction, extrusion or a

28 Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. OJ L 338,

22.12.2005, p.1-26. 29 FDA Guidance for Industry: guide to minimize microbial food safety hazards for fresh fruits and vegetables. 1998.

http://www.fda.gov/Food/GuidanceRegulation/GuidanceDocumentsRegulatoryInformation/ProducePlantProducts/ucm06

4574.htm

http://www.fda.gov/Food/GuidanceRegulation/GuidanceDocumentsRegulatoryInformation/ProducePlantProducts/ucm064574.htm

http://www.fda.gov/Food/GuidanceRegulation/GuidanceDocumentsRegulatoryInformation/ProducePlantProducts/ucm064574.htm


EFSA Journal 2014;12(12):3937 90

combination of those processes). Minimal processing may occur at harvest as well as on farm post-

harvest and at processing.

Onions (Allium cepa L.) are biennial plants of the Alliaceae family. The edible portions of the bulb

are the enlarged leaf bases and compact stem. Green onions, also called scallions, are eaten for their

immature bulb and green foliage. The predominant flavour component results from activity of the

enzyme alliinase in broken or crushed tissue, yielding the volatiles propyl disulphide and methyl

propyl disulphide. High quality onions should have mature bulbs with good firmness and compactness

of fleshy scales. The size, shape and colour of the dry skin should be typical for the cultivar. They

should be free of mechanical or insect damage, decay, sunscald injury, greening of fleshy scales,

sprouting, bruising and any other defects (Adamicki, 2014).

Pesticides cover insecticides, acaricides, herbicides, fungicides, plant growth regulators, rodenticides,

biocides and veterinary medicines. Pesticides are chemical compounds: a substance or mixture of

substances, or micro-organisms including viruses used in plant protection to: (i) kill, repel or control

pests to protect crops before and after harvest; (ii) influence the life processes of plants; (iii) destroy

weeds or prevent their growth; (iv) preserve plant products.30

Petiole is the slender stalk that attaches the leaf blade to the stem. Through evolution, the petiole

comes from the differentiation of the leaf blade and is histologically different from the stem. In some

plant species the leaves are directly attached to the stem without petiole (e.g. onion), while in others

the petiole in particularly developed (e.g. celery).

Potable water is water which meets the requirements laid down in Council Directive 98/83/EC of

3 November 1998 on the quality of water intended for human consumption (mainly microbiological

and chemical criteria) (Regulation (EC) No 852/2004).31

Post-harvest is the stage of crop production after harvest and includes on-farm cooling, cleaning,

sorting and packing.

Pre-harvest incorporates all activities on the farm that occur before crop products are harvested.

Process Hygiene Criteria are criteria indicating the acceptable functioning of the production process.

Such criteria are not applicable to products placed on the market. They set an indicative contamination

value above which corrective actions are required in order to maintain the hygiene of the process in

compliance with food law (Regulation (EC) No 2073/2005).32

Processing are any actions that substantially alter the initial product, including heating, smoking,

curing, maturing, drying, marinating, extraction, extrusion or a combination of those processes (Regulation (EC) No 852/2004).

33

Salad bar is a buffet-style table or counter sometimes at a restaurant or in a retail establishment,

although this can also be in a specific food provider. Salad components are provided for assembly,

sometimes by the customers themselves. In addition to ready-to-eat salad and other foods of non-

animal origin (including fruit and pulses), ready-to-eat meat, fish, egg products as well as bread and

cooked pasta may be available together with salad dressing.

30 Based upon definition available at http://ec.europa.eu/food/plant/plant_protection_products/index_en.htm 31 Regulation (EC) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of

foodstuffs. OJ L 139, 30.4.2004, p.1-54. 32 Commission Regulation (EC) No 2073/2005 of 15 November 2005 on microbiological criteria for foodstuffs. OJ L 338,

22.12.2005, p.1-26. 33 Regulation (EC) No 852/2004 of the European Parliament and of the Council of 29 April 2004 on the hygiene of

foodstuffs. OJ L 139, 30.4.2004, p.1-54.

http://ec.europa.eu/food/plant/plant_protection_products/index_en.htm


EFSA Journal 2014;12(12):3937 91

Sanitizers are chemical agents that reduce micro-organisms on food contact surfaces by at least

99.999 %. Within this opinion sanitizers are defined as those decontamination agents applied to reduce

the level of micro-organisms on bulb and stem vegetables and carrots.

Scales modified fleshy leaves that form concentric fleshy layers that form the bulbs. Onions are

formed by layered scales, which are the bases of the leaves of the onion plant that swell to accumulate

water and nutrients while the onion bulb matures and the upper part of the leave dries. The external,

dry, scales of the onion bulb are called tunics and protect the bulb from dehydration. Garlic is formed

by scaly scales which are modified leaves loosely clustered around the stem base.

Shoots are sprouts obtained from the germination and the development of seeds, or from the

development of buds. Depending on their development, shoots may correspond to enlarged buds,

young stem, young leaves, and cotyledons - the latter only in the case of sprouts from seeds.

Stem is the main trunk of a plant, the primary plant axis that develops buds and shoots.

Stem plate is a flat and very short stem at the basis of the onion bulb that carry the scales (bases of the

leaves) and on which the roots are attached.

Stems vegetables are plants grown for the whole stems which are used as vegetables, e.g. asparagus,

celery and rhubarb.

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